mark christie 2019 - purdue agriculture · 2021. 1. 7. · mark christie 2019 . 2 ... leaves...
TRANSCRIPT
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Mark Christie
2019
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TABLE OF CONTENTS Page
I. GENERAL INFORMATION ...........................................................................................................................4 A. Education.......................................................................................................................................................4 B. Previous Positions .........................................................................................................................................4 C. Present Position .............................................................................................................................................4 D. Awards and Honors .......................................................................................................................................4 E. Professional and Scholarly Associations ......................................................................................................4
II. LEARNING ........................................................................................................................................................5 A. Teaching Assignments at Purdue ..................................................................................................................5
B. Selected Discussion of Courses ....................................................................................................................6 C. Course Evaluation .........................................................................................................................................8
1. Student ...................................................................................................................................................8 D. Other Teaching Experience ...........................................................................................................................9 E. Other Contributions to Undergraduate Education ..........................................................................................9
III. DISCOVERY ....................................................................................................................................................10 A. Discussion of Research ...............................................................................................................................10 B. Publications .................................................................................................................................................20
1. Refereed ...............................................................................................................................................20 2. In Press .................................................................................................................................................20 3. Submitted .............................................................................................................................................23 4. In Preparation .......................................................................................................................................24 5. Book Chapters ......................................................................................................................................24 6. Book Chapters in Press ........................................................................................................................24 7. Book Reviews/Editorials .....................................................................................................................24 8. Abstracts ..............................................................................................................................................24
C. Invited Lectures...........................................................................................................................................24 1. National and International Meetings ....................................................................................................24 2. Regional Meetings and Workshops .....................................................................................................25 3. Universities and Other Institutions ......................................................................................................25
D. Other Presented Papers ...............................................................................................................................26 E. Other Professional Activities ......................................................................................................................27 F. Interdisciplinary Activities ..........................................................................................................................27 G. Patents .........................................................................................................................................................27 H. Funding .......................................................................................................................................................27
1. Discussion of Support ..........................................................................................................................27 2. Funding ................................................................................................................................................27
I. Evidence of Involvement in Graduate Research Program ..........................................................................29 1. Number of M.S. and Ph.D. Students Graduated ..................................................................................29 2. Current Graduate Students, Post doctorates, and Undergraduates ......................................................29
IV. ENGAGEMENT ............................................................................................................................................... 30 A. Discussion of Service .................................................................................................................................. 30 B. Department .................................................................................................................................................. 30 C. College of Science....................................................................................................................................... 30 D. University .................................................................................................................................................... 30 E. Professional ................................................................................................................................................. 31
1. Grant Review ....................................................................................................................................... 31 2. Editorial Board ..................................................................................................................................... 31 3. Reviewed Manuscripts ......................................................................................................................... 31 4. Reviewed Grants for agencies ............................................................................................................. 31 5. Contacted and participated on grant panels.......................................................................................... 31
F. Diversity Activities ..................................................................................................................................... 31
G. Other Engagement Activities ...................................................................................................................... 31 V. APPENDIX ....................................................................................................................................................... 34
A. Appendix A – Your 3 Year Plan .................................................................................................................34
B. Appendix B – Mentoring Section ..................................................................................................…….
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C. Appendix C – Open Discussion on Work with Undergraduates............................................................. D. Appendix D – Free Response Area.........................................................................................................
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I. GENERAL INFORMATION
A. Education 2009 Ph.D., Zoology, Oregon State University - Corvallis, OR.
2002 B.A., Biology, Cum Laude, Boston University - Boston, MA.
B. Previous Positions
2012-2014 Postdoctoral Research Fellow: University of Michigan, Ann Arbor, MI.
Genetic effects of habitat connectivity on long-term population persistence;
emphasis on modeling and Approximate Bayesian Computation.
L. Lacey Knowles advisor
2010-2014 Postdoctoral Research Fellow: Oregon State University, Corvallis, OR.
Research on the effects of salmon hatcheries on wild populations.
Michael S. Blouin advisor
2003-2009 Research Assistant: Oregon State University, Corvallis, OR.
Research on the dispersal and recruitment of marine fishes.
Mark A. Hixon advisor
2004-2005 Field Assistant: Lee Stocking Island, Bahamas.
Assisted with ongoing sampling and experiments of coral-reef fish ecology.
2002-2003 Research Associate: Exact Sciences Biotech, Boston, MA.
Performed molecular work to optimize novel genetic approaches for diagnosing
cancer.
2001-2002 Research Assistant: New England Aquarium, Boston, MA.
1999-2002 Research Assistant: Boston University Marine Program and Marine Biological
Laboratory, Woods Hole, MA.
C. Present Position 2014-Present Assistant Professor, Department of Biological Sciences & Department of Forestry
and Natural Resources, Purdue University, West Lafayette, IN
D. Awards and Honors
E. Professional and Scholarly Associations
American Genetic Association
American Society of Ichthyologists and Herpetologists
Ecological Society of America
International Society of Computational Biology
Society for the Study of Evolution
Western Society of Naturalists
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II. LEARNING
A. Teaching Assignments at Purdue (Written by Candidate)
Semester Year Course # Title, Credit, Type Enroll. Student
Classification
Fall 2015 FNR 241 Ecology & Systematics of
Fishes, 3 credits
84 Undergraduate
Spring 2016 BI 58000 Evolution, 3 credits
18 Senior/Graduate
Spring 2016 BI 65300 Advanced Evolution Discussion, 1 credit
7 Graduate
Spring 2016 BI 59500 Genomics in Ecology and Evolution, 1 credit
9 Graduate
Fall 2016 FNR 24150 Ecology & Systematics of Fishes, 3 credits
87 Undergraduate
Fall 2016 BI65200 Advanced Ecology & Evolution Discussion, 1 credit
11 Graduate
Spring 2017 BI 58000 Evolution, 3 credits
21 Undergraduate & Graduate
Spring 2017 BI 69500 Writing in Ecology & Evolution, 1 credit
6 Graduate
Fall 2017 FNR 24150 Ecology & Systematics of Fishes, 3 credits
81 Undergraduate
Fall 2017 BI65200 Advanced Ecology & Evolution Discussion, 1 credit
4 Graduate
Spring 2018 BI 58000 Evolution, 3 credits
37 Undergraduate & Graduate
Spring 2018 BI 69500 Writing in Ecology & Evolution, 1 credit
4 Graduate
Fall 2018 FNR 24150 Ecology & Systematics of Fishes, 3 credits
93 Undergraduate
Spring 20019 BI 58000 Evolution, 3 credits
32 Undergraduate & Graduate
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B. Selected Discussion of Courses (Written by Candidate)
FNR24150
The ecology and systematics of fishes and herptiles provides a general overview of two dominant
vertebrate taxa. The course is a requirement for all Forestry and Natural Resource students and
enrollment in some years can exceed 90 students. Most students taking the class are sophomores.
I teach the fishes portion of this course (1/2 semester) for fulfillment of my 25% appointment in
the Department of Forestry and Natural Resources. This course is rewarding, but it is a challenge
to present an overview of all 33 thousand extant fishes within half a semester. As such, I mainly
focus on broad phylogenetic relationships and draw upon examples from specific species
throughout. When I arrived at Purdue, this course was taught with hierarchical, taxonomic
relationships. I quickly transitioned to using modern phylogenetic relationships among fishes,
which simultaneously requires students to understand phylogenetic methods and to understand
the evolutionary relationships among an immensely diverse group of vertebrates. For many
students, this course is their first exposure to evolution.
Because of time constraints, this course mostly focuses on extant species. The course
begins with jawless fishes (agnathans), moves on to chimaeras, sharks, and rays
(Chondrichthyes), and then progresses to bony fishes (Osteichthyes). Within the osteicthyes we
focus on Sarcopterygii and the evolution of terrestrial vertebrates before spending a considerable
portion of the class reviewing the diversity found within the ray finned fishes (Actinopterygii).
Beyond the phylogenetic relationships, I also provide an overview of swimming mechanics,
ectothermy (and regional endothermy), respiration, osmoregulation, buoyancy, sensory systems,
schooling, feeding ecology & behavior, reproduction, early life history, growth, population and
community ecology, fish genetics, and conservation.
I begin each class with a “Fish of the Day”,
which features a fish that I find particularly
interesting. We first review the phylogenetic
placement of the fish (where does it fit in relation to
other fishes) and then I present a suite of interesting
facts about the fish. For example, south American
leaf fish not only look like different stages of dead
leaves (figure 1), individuals act like dead leaves too
and use this camouflage to hunt prey and escape
predation. I also use “think-pair-share” activities in
every lecture, where I propose a big picture, often
conceptual question, ask the students to talk it over
with their neighbors for 1-2 minutes, and then ask
Figure 1: South American leaf fish (Monocirrhus polyacanthus) look and act like dead and decaying leaves.
for volunteers to present their answers. Because the questions are largely conceptual, there is
often no one correct or incorrect answer. The students quickly realize that there is little risk with
offering unusual answers and participation in this portion of the lecture is considerably higher
then I expected when I first trialed this activity. The student’s creativity in their answers have in
many cases resulted in diverse solutions to complex problems – such that I have started writing
many of them down for further exploration. Lastly, I include lots of short videos showing fishes
in their natural environments – many of these videos focus on marine fishes and it is rewarding
to watch the students’ eyes opened to entirely new worlds.
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BIO58000
“Nothing in biology makes sense except in the light of evolution” - Theodosius Dobzhansky
“Nothing in evolution makes sense except in the light of population genetics” - Michael Lynch
Evolution is the only upper level evolution course offered at Purdue University. This course
introduces students to fundamental and advanced concepts in evolutionary biology including
population genetics, natural selection, genetic adaptation, and speciation. Because nothing in
evolution makes sense except in the light of population genetics, each semester is begun with a
comprehensive introduction to this field. Population genetics has a rich mathematical history, but
I find that simply presenting a series of equations, while illuminating for some students, leaves
the vast majority of students confused or completely in the dark. Consequently, I have developed
a comprehensive set of individual-based models that illustrate each of the four fundamental
evolutionary forces that affect allele frequencies: genetic drift, mutation, gene flow, and natural
selection (figure 2). Each
module is written in R and
because enrollment in this
class is capped at 30 students,
we can use the 16
departmental laptops to allow
students to work in class in
groups of two. Parameters are
set at the beginning (i.e., the
top) of each script and include
variables such as population
size, initial allele frequency,
mortality rate etc. The code
for each of the modules is
appended below the
parameters and, for extra
credit, I allow students to
modify the code to identify
answer questions the
presented model cannot (e.g., Figure 2: Screen shot illustrating one of the R modules designed to illustrate the effects of genetic drift. Each point represents an individual and each color represents the allele of that individual. Allele frequencies can be identical at the start of the simulation (a shown here) or varied by the student along with carrying capacity, number of offspring per pair, and dispersal strategy.
responses at multiple, linked
loci). All of the code is
available on our lab website
and our lab GitHub repository.
After obtaining an introduction in population genetics, the course moves on to cover topics
in domestication, rapid evolution, microevolution, speciation, sexual selection, life history
evolution, and phenotypic evolution. We also discuss the role and application of genomics and
bioinformatics to modern evolutionary analyses. Because this course convenes for 75 minutes
twice per week, I typically lecture for the first 30-40 minutes and then spend the remainder of the
class time with active learning activities. Aside from working with R scripts we discuss relevant
papers as a class, present figures from papers to the class (in groups of 4-5), design theoretical
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experiments in small groups, review papers on bioRxiv, present on evolution in the news, and
work with new bioinformatics software.
I find the large amounts of group work undertaken in this course to be particularly
enjoyable. When groups of 2-5 students are working together I always walk around and provide
feedback and additional information when needed; it is particularly rewarding to hear students
coming up with novel questions, unique experimental designs, and problem-solving strategies.
When I first took over this course, the format consisted of straightforward lecturing with time for
occasional questions. While I think this strategy was effective for some students, the gradual
transition to a highly interactive classroom has been one of my most rewarding teaching
accomplishments. Future development will include greater exposure of students to coding,
refinement of lecture material, and the continued trialing and implementation of various active
learning exercises.
C. Course Evaluation
Evaluations of past courses are summarized below. Two values are reported for courses that
contained two sections. “Course” refers to answers to the prompt, “Overall, I would rate this
course as,” while “instructor” refers to answers to the prompt, “Overall, I would rate this
instructor as.” These values are out of a possible score of 5 where 5 = ‘Excellent’, 4 = ‘Good’,
3=’Fair’, 2=’Poor”, and 1 = ‘Very Poor’.
Fall 2015: FNR24150
Course: 4.0
Instructor: 3.9
Spring 2016: BI 58000
Course: 4.1
Instructor: 4.2
Fall 2016: FNR 24150
Course: 4.3
Instructor: 4.0
Spring 2017: BI 58000
Course: 3.8
Instructor: 4.3
Fall 2017: FNR 24150
Course: 4.5
Instructor: 4.3
Spring 2018: BI 58000
Course: 4.1 (mode 4)
Instructor: 4.6 (mode 5)
Fall 2018: FNR 24150
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Course: 4.3 (mode 4)
Instructor: 4.4 (mode 4)
D. Other Teaching Experience:
Guest Lectures:
Survey of Mathematical Biology (BTNY 560) Purdue University 2018
Fish and Wildlife Forensics (FNR 59800) Purdue University (West Lafayette, IN) 2017
Demystifying Mathematical Models (BTNY 590) Purdue University 2017
Fish and Wildlife Forensics (FNR 59800) Purdue University (West Lafayette, IN) 2016
Fish and Wildlife Forensics (FNR 59800) Purdue University (West Lafayette, IN) 2015
Evolution (BIOL 58000) Purdue University (West Lafayette, IN) 2015
Freshman Honors Biology Seminar (BI 19700) Purdue University 2015
Evolution (EEB 516) University of Michigan (Ann Arbor, MI) 2013
Ecology (BI 370) Oregon State University (Corvallis, OR) 2011
Ichthyology (FW 315) Oregon State University (Corvallis, OR) 2009-2011
Marine Ecology (Z352) Oregon State University (Corvallis, OR) 2005-2007
Graduate Teaching Instructor 2002-2009
Marine Ecology
Oregon State University (Corvallis, OR)
- lead lectures for recitations and laboratories (including field trips)
(Z352, 2 terms, 24 students)
Introductory Biology (BI 212, 2 terms, 4 sections, 200 students)
Oregon State University (Corvallis, OR)
lead lectures for recitations and laboratories
Vertebrate Zoology (BI 302, 2 sections, 84 students)
Boston University (Boston, MA)
lead laboratory sections
Workshops, Oregon State University (Corvallis, OR) 2008
Center for Genome Resources and Biocomputing
R Workshop for Statistical Computing
E. Other Contributions to Undergraduate Education
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Completed mentoring one honors undergraduate, Abigail Perkins, who conducted
independent research on the sea lamprey project. She is currently employed at IUPUI as a
research associate. Two additional undergraduate students have now also joined the lab
and are working on projects related to bioinformatics and experimental design.
Mentored two undergraduate biology majors during the 2014-2015 school year. Each
student completed an independent research project.
III. DISCOVERY
A. Discussion of Research (Written by Candidate)
Our planet is changing at an unprecedented pace and scale with large impacts to terrestrial and
aquatic ecosystems. For example, global climate change is creating widespread and often
extreme environmental changes that will have profound impacts on ecological communities.
Entire ecosystems, such as coral-reefs, are in severe peril due to increasing temperatures, rising
water levels, and ocean acidification all of which are triggered by changing climatic conditions
(figure 1), and recent studies have suggested that coral-reefs may go extinct within the next 30-
50 years. With such large-scale and high-impact environmental changes, ecologists and
evolutionary biologist are faced
with a pressing question: Can
species adapt to rapid
environmental change? This
single question is the central focus
of my research program because
the answers will guide future
conservation and management
actions for the next generation. If a
species cannot keep pace with Figure 1: Healthy reef-building acroporid coral (left photo) versus colonies of bleached corals (right photo). High water temperatures, which cause corals to expel their symbiotic algae required for photosynthesis, in combination with rising water levels and increased ocean acidification are threatening coral reef ecosystems.
projected environmental changes,
then extinction is the likely
outcome in the absence of direct
intervention (e.g., captive
breeding).
Understanding which species can rapidly adapt to novel environmental changes and how
they are able to adapt may allow us to better predict which species can be managed in situ. Given
that a response to selection requires a heritable trait, it may be that some genomic properties are
good predictors of adaptive ability; genome-wide estimates of genetic diversity, recent genome
duplication events, and areas of high recombination all represent possible predictors of adaptive
ability. The power of and promise of genetic tools is high, but much more work needs be
accomplished before we can begin to build a predictive framework for understanding which
species can adapt to environmental change.
To that end, my research focuses three themes related to whether species can keep pace
with rapid environmental change and all three themes focus on genetic adaptation to novel
conditions: 1. rapid genetic adaptation of introduced species to novel environments, 2. rapid
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genetic adaptation to xenobiotic compounds, and 3. rapid genetic adaptation to captivity.
Although I often focus on the outcomes of selection, additional evolutionary forces, such as
genetic drift and gene flow feature prominently in these three themes. My work has primarily
focused on fishes, but is largely question driven and thus focused on diverse taxa ranging from
schistosomes to southern right whales and banner-tailed kangaroo rats.
1: Rapid genetic adaptation of introduced species to novel environments.
Understanding how introduced species can adapt to novel environments provides a useful
framework for understanding adaptive evolution because in many cases species are predicted to
have large shifts in their geographic ranges outside of their current, native boundaries.
Work in my lab has focused on two non-native species - the introduced steelhead trout
(Oncorhynchus mykiss; figure 2) and the invasive sea lamprey (Petromyzon marinus; figure 5) -
both of which now occur in the Laurentian Great Lakes. The Great Lakes are an ideal location
for studying rapid genetic adaptation to novel environments due to the diverse habitats and
relatively recent colonization events for most non-native species.
Steelhead trout are an ecologically, economically, and culturally important fish that are
native to the northern Pacific and surrounding regions. Steelhead exhibit an extraordinary
amount of life history variation both within and among populations. In fact, two alternative life
history variants - the ocean-going, anadromous steelhead and the stream-residing resident
rainbow trout - are so phenotypically divergent that they were once classified as separate species
(figure 2), though my work and others have established that these life history variants routinely
interbreed with one another. In fact, two freshwater resident fish can produce ocean-going
steelhead progeny and vice versa (Christie et al. 2011). There is also extensive life history
variation within just the ocean-going, anadromous steelhead. Some steelhead are semelparous;
they spawn once and die. Semelparous steelhead may return to spawn at different ages (2-5 years
old), spending various amounts
of time in freshwater or marine
habitats. Other steelhead, known
as repeat spawners or kelts,
spawn two and sometimes three
times in their lifetime, returning
to the ocean between each
spawning event. Furthermore,
some steelhead mature in the
ocean before returning to rivers
to spawn (e.g., winter-run
steelhead), while others return
early and overwinter in
Figure 2: Mature resident male O. mykiss (top) next to an ocean-
returning steelhead male (bottom). Ocean-going males are considerably larger than their resident counterparts. In the Great Lakes, only the larger steelhead phenotype is documented. Photo courtesy of J. McMillan.
freshwater before spawning (e.g.,
summer-run steelhead). Recent
work in my lab has revealed that
many of these distinct life history
strategies are maintained by a
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Figure 3: Comparison of pooled heterozygosity (HP) across chromosomes and between populations. Mean HP,
averaged across 25 100 kb windows, is illustrated by the solid lines. The 95% confidence interval around each mean is illustrated with shading
combination of fitness trade-offs, where a fitness benefit associated with one function (e.g., size
at reproduction) is correlated with a fitness cost of another function (e.g., survivorship) and
negative frequency dependent selection, where the relative fitness of a particular life history
strategy declines as the life history strategy increases in frequency (Christie et al. 2018).
Both steelhead and rainbow trout, have been widely introduced throughout the world. In
the late 1890s, steelhead from northern California were introduced into Lake Michigan and
natural reproduction was documented shortly thereafter. In their native range, most steelhead
spend the first one to two years of their lives in freshwater streams before migrating out to the
ocean to forage and grow. By contrast, steelhead from Lake Michigan continue to spawn in
streams and rivers, but now use the entirely freshwater environment of the Great Lakes as a
surrogate ocean. Furthermore, there is no known interbreeding between resident and anadromous
life history variants in Lake Michigan (i.e., steelhead and resident rainbow trout are not, to our
knowledge, sympatric), suggesting that steelhead have adapted to the novel freshwater
environment. Apart from salinity, there are many additional differences between the introduced
and native habitats including water temperature, stream characteristics, and community
composition. Beginning in the mid-1980s, hatchery fish of diverse ancestry were released into
Lake Michigan, and their high survival rates allowed for possible introgression with the original,
California-derived strain. To examine the genetic effects of this introduction, we sequenced the
entire genomes of 264 fish using fish collected from the ancestral range in California, fish from
Lake Michigan in the early 1980’s (before the possible hatchery introgression), and fish from the
late 1990’s (after hatchery introgression) (Willoughby et al. 2018).
In all three populations, genetic diversity was lowest at the centromeres and contained a
region with extremely high heterozygosity on chromosome 5 (Figure 3), subsequently identified
as an inversion associated with an anadromous life history in steelhead. When making
comparisons between the California population and the Lake Michigan samples we found three
striking patterns (Figure 3): First, heterozygosity in the ancestral California population was
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Figure 4: SNPs and functions associated with the outlier region on chromosome 4. A) FST for all SNPs located within the outlier region, denoted by the extent of the black bracket, for both California vs. Lake Michigan 1983 and California vs. Lake Michigan 1998. Highlighted regions display the extent of the two genes located within the outlier region: 1. gram domain containing 4 (GRAMD4); and 2. ceramide kinase (CERK). (B) For all SNPs with large allele frequency changes found within CERK, we compared allele frequency of the major allele in the 1983 Lake Michigan population between the California, Lake Michigan 1983, and Lake Michigan 1998 populations. Many SNPs show evidence of positive selection favoring a previously rare allele, including 5 SNPs that resulted in non- synonymous changes (orange lines). The orange box displays the function of CERK: a kinase that phosphorylates ceramide, forming ceramide-1-phosphate (C-1-P), which then activates DNA synthesis, cell division, and wound-repair pathways. In both A and B, each short vertical, black line depicts the location of a single exon within the gene.
higher than heterozygosity in the Lake
Michigan across all chromosomes. In fact,
Lake Michigan 1983 steelhead were
characterized by a 9.5% reduction in
genetic diversity across the entire genome.
Second, we found that average
heterozygosity in the 1998 Lake Michigan
population was higher than heterozygosity
in the 1983 Lake Michigan population,
resulting in a mean 4.8% increase in
genetic diversity between 1983 and 1998,
a pattern which reflects the successful
introgression of hatchery-stocked smolts.
Lastly, we observed that the reduction in
heterozygosity in the Lake Michigan
populations relative to California
depended on position along each
chromosome. This pattern was not driven
by changes in the total number of SNPs,
read depth, occurrence of paralogous loci,
gene density, or number of repetitive
elements. Thus, the present-day
distribution of genetic diversity in Lake
Michigan steelhead likely reflects the
evolutionary interplay among gene flow
(here introgression from hatchery strains),
recombination, and purifying selection.
By examining genes in regions with
high genetic differentiation between the
California and Lake Michigan population,
we found evidence of selection in
osmoregulatory and acid-base balancing
pathways on two independent
chromosomes. We also found evidence of
selection that altered metabolic processes
were associated with the genetic
adaptation of steelhead to the Great Lakes
(Figure 4). The selection on CERK and
the associated modulation of C-1-P
induced cell proliferation suggests
steelhead metabolism played an important
role in adaptation to the freshwater
environment. This adaptation may have
allowed steelhead to take advantage of
alternative prey or allocate additional
resources to activity in the Lake Michigan habitat. Intriguingly, C-1-P greatly increases the DNA
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synthesis of fibroblasts, cells that play a key role in wound healing pathways (Gomez-Muñoz et
al., 1995, 1997; Singer & Clark, 1999). In the Great Lakes specifically, introduced, parasitic sea
lamprey occur at high densities, and lamprey attacks result in large wounds resulting in mortality
rates of ~40% parasitized O. mykiss individuals. Most lamprey species that exist in the native
steelhead range are non-parasitic and parasitic Pacific lamprey occur at much lower densities
than Lake Michigan sea lamprey and do not rely heavily on salmon as hosts. Thus, we speculate
that C-1-P mediated wound healing may be a response to the strong selective pressure imposed
by introduced parasitic sea lamprey found at high abundances in Lake Michigan. Future work in
my lab will investigate the possibility of rapid coevolution between introduced steelhead and
invasive sea lamprey.
By comparing Lake Michigan steelhead to their ancestral population, we were able to
uncover genomic patterns of rapid genetic adaptation to the Great Lakes ecosystem despite a
reduction in genome-wide genetic diversity. That genetic adaptation can still occur despite
genome-wide reductions in genetic diversity has substantial conservation and management
implications; imperiled species with small population sizes may still be able to adapt to changing
environmental conditions. Using genomic approaches to better understand which genes,
populations, and species can rapidly respond to novel and often anthropogenically-induced
selective forces represents a key component of future of conservation research.
2. Rapid genetic adaptation to xenobiotic compounds
The rapid evolution of resistance to xenobiotic compounds has been widely documented in
microbes, fungi, invertebrates, and plants. Resistance has also been documented in vertebrates
but has largely been constrained to taxa with high fecundity and short generation times.
Nevertheless, the fundamental principles governing the evolution of resistance still apply to
species with longer generation times. If the selection pressure imposed by a xenobiotic is strong,
wide-spread, and consistently applied year after year, then resistance may still evolve. One such
possibility occurs throughout the Great Lakes, where a powerful chemical lampricide has been
applied to control invasive sea lamprey (Petromyzon marinus) for over 60 years. Because the
lampricide kills most, but not all, larval sea lamprey, it is possible that some individuals are able
to survive exposure. If this process is repeated over a long enough period, then resistant
individuals could increase in frequency – a scenario documented in many systems where pests
have been controlled by chemical means. The evolution of resistance would greatly reduce the
effectiveness of the lampricide, which remains the primary control agent, and could result in
Figure 5: Larval stage sea lamprey (Petromyzon marinus), known as ammocoetes, do not have functional eyes and remain buried in the substrate before transforming into parasitic adults. The parasitic adults use their circularly- arrayed teeth to attach to host fishes. The two photos of ammocoetes were taken by an undergraduate journalism/biology double major, Scott See, who worked in our lab.
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large declines to native fish populations due to increases in lamprey abundance. These declines
in fish abundance would not only have large ecological repercussions but could also result in
billions of dollars in economic damage.
Invasive sea lamprey impact native populations and communities by wounding and often
killing the host fishes that they parasitize. Following their invasion into the Laurentian Great
Lakes (hereafter Great Lakes) in the late 1930s, sea lamprey contributed to the catastrophic loss
of economically valuable commercial and recreational fisheries in Canada and the United States.
In response to the proliferation of sea lamprey throughout the Great Lakes, there was an
immediate and concerted effort to develop efficient means of control. One effort, initiated in the
1950s, involved testing over 6,600 chemical compounds on sea lamprey and other fish species.
The organic compound 3-trifluoromethyl-4-nitrophenol (hereafter TFM) was found to effectively
kill larval sea lamprey and had few detectable effects on other fish species at low concentrations.
TFM control was highly successful and sea lamprey abundance was reported to have been
reduced by approximately 90%, resulting in recovery of economically important fisheries. This
outcome is one of the few documented cases of an invasive vertebrate species being successfully
controlled by a pesticide. Alternative control measures have been implemented on smaller scales,
but none have proven as effective as TFM. Thus, there is a continued reliance on TFM to
manage invasive sea lamprey
populations in the Great
Lakes. This reliance on a
single control measure can be
risky; only a handful of
manufacturers produce TFM
(because the only known
application is as a lampricide)
and thus both prices and
supplies of TFM could change
(Dunlop et al. 2017). More
importantly, reliance on a
single chemical control
measure has been shown in
other pests to drastically
increase the chances of
resistance evolution.
Figure 5: Effects of costs of resistance on the evolution of resistance. Panels A and B illustrate the relationship between the cost of resistance and the number of resistant larvae through time. TFM treatment was started in year 50 (black vertical line), a single resistant adult was added in year 70 (blue vertical line) and TFM treatment was stopped in year 100 (red vertical line). When there is no cost of resistance (panel A), the number of resistant larvae does not decline through time even after TFM treatment is stopped. When cost of resistance is moderate (10% reduction in fitness, panel B), the number of resistant larvae gradually declines through time. Panel C illustrates the proportion of resistant larvae as a function of years until detection where cost of resistance was varied from 0 to 0.5 (see legend). Panel D illustrates the trade-off between the proportion of parasites killed by TFM and the probability of resistance evolving examining three costs of resistance (colors match the legend in panel C).
In order to determine
when resistance is likely to
evolve and to examine the
factors that can expedite or
delay the onset of resistance,
we constructed an eco-genetic
model that mimics the unique
life history of sea lamprey
(Figure 5). We found that
resistance alleles rapidly rise
to fixation after 40-80 years of
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treatment. The absence of natal homing allows resistant individuals to spread quickly throughout
the entire system making detection challenging while simultaneously increasing the overall
likelihood of resistance evolving. High costs of resistance and density independent reproduction
can delay, but not prevent, the onset of resistance (Figure 5). The results of this research
illustrate that sea lamprey have the potential to evolve resistance to their primary control agent in
the near future, highlighting the urgent need for alternative control strategies.
In my lab we often combine theoretical work with empirical work. Towards the empirical
end we have performed extensive toxicology and gene expression work on larval lamprey from
their introduced and native ranges. We obtained a total of 1451 live sea lamprey (Petromyzon
marinus) ammocoetes collected from three locations: 1. Lake Michigan, 2. Lake Champlain, 3.
Connecticut. Lake Michigan has been treated with TFM for 59 years, Lake Champlain for 32
years, and Connecticut for 0 years (native range). Larvae were acclimatized for a minimum of
four months before the first exposure to TFM to minimize environmental effects.
We found no differences in survivorship between larvae from the native range and larvae
from TFM-treated portions of the range after exposure to TFM. However, we did detect large
differences in gene expression between individuals exposed to sub-lethal concentrations of TFM
where 197 genes were differentially expressed (most of which were upregulated) in larvae
collected from Lake Michigan with only 5 and 13 genes differentially expressed in Connecticut
and Lake Champlain, respectively, suggesting a different response among populations (Figure 6).
We are currently in the process of identifying the pathways and specific functions of these 197
genes, but these data suggest that Lake Michigan lamprey may have evolved resistance to
sublethal exposure to TFM and may be in the initial stages of evolving lethal resistance.
Functionally, most of
the genes are involved
in increasing the
production of ATP,
which validates the
previously confirmed
mode of action for
TFM. To further
confirm these
preliminary results,
we have just finished
sequencing 56 more
samples consisting of
29 muscle tissue, 19
liver tissue, and 8
brain tissue.
Figure 6: Patterns of gene expression between sea lamprey larvae exposed to sub- lethal concentrations of the lampricide TFM in comparison to control (unexposed) larvae from the same populations. A total of 197 genes were differentially expressed in larvae from Lake Michigan in comparison to 5 from Lake Champlain and 13 from Connecticut, suggesting a different response among populations
3. Rapid genetic adaptation to captivity
Captive environments are often strikingly different than those found in the wild. As such,
understanding how species can rapidly adapt to captivity can provide insights into how and why
rapid genetic adaptation occurs. Additionally, if species cannot adapt to changing environmental
conditions captive breeding programs may represent a last resort. Thus, one goal of captive
breeding programs is to bolster threatened or endangered populations. Yet these programs often
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produce individuals that are maladapted upon reintroduction into the wild. Captive breeding on a
massive scale is exemplified by the more than six billion hatchery-raised salmon that are
intentionally released each year into the Northern Pacific ecosystem. I am currently leading a
multidisciplinary project to investigate the genetic impacts of releasing hatchery steelhead
(Oncorhynchus mykiss) into the wild. Despite having wild-origin fish as parents, it was unclear
why hatchery fish had substantially lower reproductive success in the wild than their wild-born
counterparts. To address this unknown, I reconstructed pedigrees for three generations of fish
(13,000 fish from 15 years), and determined that hatchery fish were unexpectedly adapting to the
captive environment in a single generation. These results demonstrate that a single generation
in captivity can result in a substantial response to selection on traits that are beneficial in
captivity, but severely maladaptive in the wild (Christie et al. (2012b), PNAS; highlighted in
NPR, NY Times, and Faculty of 1000). This finding of rapid genetic adaptation represents a
general phenomenon found in many first-generation hatchery salmon species and populations,
and thus has major implications for the viability of threatened fish populations (Christie et al.
2014).
My salmon research is also uncovering complex tradeoffs that arise with any
supplementation and captive breeding program. For example, by combining novel pedigree and
population genetic analyses, I was able to determine that supplementation programs can reduce
the effective population size of an entire population by nearly two-thirds (Christie et al. 2012a).
This work on hatcheries also revealed that the loss in genetic diversity was greatest when (1)
more hatchery fish were allowed onto the spawning grounds and (2) the reproductive success of
returning hatchery fish was high. These findings suggest that explicitly accounting for the
demographic, genetic, and societal costs and benefits of supplementation could pave the way for
more prudent management actions. Recent theoretical work in my lab has addressed the long-
term demographic and genetic effects associated with releasing captive-born individuals with
varied life histories into the wild (Willoughby and Christie 2017, 2018). We developed eco-
genetic models for four species with long-running captive-breeding and release programs: coho
salmon (Oncorhynchus kisutch), golden lion tamarin (Leontopithecus rosalia), western toad
(Anaxyrus boreas), and whooping crane (Grus americana). We found that releasing even slightly
less fit captive-born individuals to supplement wild populations can result in reductions in
population sizes and genetic diversity over the long term, provided that the fitness reductions are
heritable (i.e., due to genetic adaptation to captivity) and that the populations continue to be
regulated by density-dependent mechanisms. Species with longer life spans and lower rates of
population replacement experienced smaller negative effects than those with shorter life spans
and higher rates of population replacement. Furthermore, programs that released captive-born
individuals over fewer years or that could avoid breeding individuals with captive ancestry
experienced smaller reductions in population size and genetic diversity over the long term.
Relying on selection in the wild to remove individuals with reduced fitness mitigated some
negative demographic effects, but at a substantial cost to neutral genetic diversity. These recent
results suggest that conservation-focused captive breeding programs should take measures to
prevent even small amounts of genetic adaptation to captivity, quantitatively determine the
minimum number of captive-born individuals to release each year, and fully account for the
interactions among genetic adaptation to captivity, population regulation, and life history
variation
Ongoing work in this research area includes (1) determining the specific genes and traits
that are under selection in the hatchery, (2) examining the ongoing role of life-history variation
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in rapid genetic adaptation, and (3) determining whether the lack of mate choice in captivity can
contribute to the production of offspring that have reduced fitness in the wild (e.g., inbreeding,
sexual selection, MHC genes).
Future work [work in progress – add yellow perch stuff; DNR stuff]
Ongoing and future work in my lab focuses on each of the three broad topics discussed above.
My lab is expanding our sea lamprey research to identify the timing and potential genetic
mechanisms of resistance and to identify the rapid co-evolution among invasive sea lamprey and
introduced salmonids. We are also expanding our study systems to identify further generalities of
rapid genetic adaptation to novel environments. For example, we are examining rapid genetic
adaptation to the Great Lakes with pink salmon, which have a well-documented progenitor
population (samples obtained in collaboration with Lisa and Jim Seeb). We are also investigating
the possibility of genetic adaptation to thiamine (vitamin B1) poor diets that afflict some salmon
populations, which may become an emerging conservation issue. With increasing empirical
observations of rapid adaptive evolution, occur our central aim is to develop a unified framework
for contemporary evolution. Such a framework will be used to guide the ongoing conservation
and management of threatened and imperiled populations.
Literature cited:
Christie, M. R., M. J. Ford, and M. S. Blouin. 2014. On the reproductive success of early‐
generation hatchery fish in the wild. Evolutionary Applications 7:883-896.
Christie, M. R., M. Marine, R. French, R. S. Waples, and M. Blouin. 2012a. Effective size
of a wild salmonid population is greatly reduced by hatchery supplementation.
Heredity 109:254.
Christie, M. R., M. L. Marine, and M. S. Blouin. 2011. Who are the missing parents?
Grandparentage analysis identifies multiple sources of gene flow into a wild
population. Molecular Ecology 20:1263-1276.
Christie, M. R., M. L. Marine, R. A. French, and M. S. Blouin. 2012b. Genetic adaptation
to captivity can occur in a single generation. Proceedings of the National
Academy of Sciences 109:238-242.
Christie, M. R., G. G. McNickle, R. A. French, and M. S. Blouin. 2018. Life history
variation is maintained by fitness trade-offs and negative frequency-dependent
selection. Proceedings of the National Academy of Sciences:201801779.
Dunlop, E. S., R. McLaughlin, J. V. Adams, M. Jones, O. Birceanu, M. R. Christie, L. A.
Criger, J. L. Hinderer, R. M. Hollingworth, and N. S. Johnson. 2017. Rapid
evolution meets invasive species control: the potential for pesticide resistance in
sea lamprey. Canadian Journal of Fisheries and Aquatic Sciences 75:152-168.
Willoughby, J. R., and M. R. Christie. 2017. Captive Ancestry Upwardly Biases
Estimates of Relative Reproductive Success. Journal of Heredity 108:583-587.
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Willoughby, J. R., and M. R. Christie. 2018. Long‐term demographic and genetic
effects of releasing captive‐born individuals into the wild. Conservation
Biology.
Willoughby, J. R., A. M. Harder, J. A. Tennessen, K. T. Scribner, and M. R. Christie.
2018. Rapid genetic adaptation to a novel environment despite a genome‐wide
reduction in genetic diversity. Molecular Ecology.
B. Publications
I have published in the following journals listed in order of the most recent impact factor (ISI
Web of Knowledge): Nature Communications (11.6), Proceedings of the National Academy of
Sciences USA (9.8), Molecular Ecology (6.3), Conservation Biology (5.9), Molecular Ecology
Resources (5.6), Ecology (5.2), Evolution (4.7), Bioinformatics (4.6), Evolutionary Applications
(4.6), PLoS Neglected Tropical Diseases (4.5), Heredity (3.8), PLoS One (3.5), Reviews in Fish
Biology & Fisheries (3.2), Oecologia (3.1), ICES Journal of Marine Science (2.9), Canadian
Journal of Fisheries and Aquatic Sciences (2.8), Ecology & Evolution (2.5) Marine Genomics
(2.0) , Journal of Heredity (1.9), Environmental Biology of Fishes (0.914)
Publications co-authored with undergraduate students, graduate students, and post-doctoral
researchers are superscripted with U, G, and P, respectively. In the fields of ecology and
evolution, the first and last author positions have the greatest significance, where first author
typically denotes the individual who performed the majority of analytical work (e.g., data
collection, data analysis) and the last author position denotes the individual whose lab the work
came from. There are exceptions, particularly when all co-authors are professors (or similar), and
cases in which I was the first author, but where the work originated from my lab are designated
with an asterix (*). Text in blue font represents perspectives and coverage of the publication
written by un-affiliated persons.
1. Refereed
34. Willoughby JRP, Waser PM, Brüniche-Olsen A, Christie MR (2019) Inbreeding load
and inbreeding depression estimated from lifetime reproductive success in a small, dispersal-
limited population. Heredity. In press.
33. Harder AMG, Ardren WR, Evans AN, Futia MH, Kraft CE, Marsden JE, Richter CA,
Rinchard J, Tillitt DE, Christie MR (2018) Thiamine deficiency in fishes: causes,
consequences, and potential solutions. Reviews in Fish Biology and Fisheries 28:865-886.
32. Martinez ASG, Willoughby JRP, Christie MR (2018) Habitat type and life history
variation determine genetic diversity in fishes. Ecology and Evolution 8:12022-12031.
31. Willoughby JRP, Christie MR. Long-term demographic and genetic effects of releasing
captive-born individuals into the wild. Conservation Biology (In press).
Perspective by Jake Buehler: “Releasing captive-bred animals has long-term drawbacks.”
Frontiers in Ecology and the Environment 16(9):492-493.
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30. Willoughby JRP, Harder AMG, Tennessen JA, Scribner KT, Christie MR (2018) Rapid
genetic adaptation to a novel environment despite a genome-wide reduction in genetic
diversity. Molecular Ecology 27:4041-4051.
Perspective by Lisa Seeb, Garrent McKinney, and Jim Seeb: “Chromosomes and genes,
spawned these fateful scenes: rapid adaptation in an introduced fish”. Molecular Ecology
(In press).
Highlighted in Science Magazine (AAAS): “This saltwater trout evolved to live in
freshwater—in just 100 years.” doi:10.1126/science.aau3582.
29. Johnson, DW, Christie MR, Pusack TJ, Stallings CD, Hixon MA (2018) Integrating
larval connectivity with local demography reveals regional dynamics of a marine
metapopulation. Ecology 99: 1419-1429.
28. Christie MR*, McNickle GG, French RA, Blouin MS (2018) Life history variation is
maintained by fitness trade-offs and negative frequency dependent selection. Proceedings of
the National Academy of Sciences 115:4441-4446.
27. Christie MR, Searle CL (2018). Evolutionary rescue in a host-pathogen system results in
coexistence not clearance. Evolutionary Applications 11:681-693.
26. Willoughby JRP, Christie MR (2017) Captive ancestry upwardly biases estimates of
relative reproductive success in supplemented populations. Journal of Heredity 108:583-
587.
25. Christie MR*, Miermans PG, Gaggioti OE, Toonen RJ, White C (2017) Disentangling
the relative merits and disadvantages of parentage analysis and assignment tests for inferring
population connectivity. ICES Journal of Marine Science 74:1749-1762.
Contribution to Themed Section: “Beyond ocean connectivity: new frontiers in early life
stages and adult connectivity to meet assessment and management”.
24. Dunlop, ES, McLaughlin R, Adams JV, Jones M, Birceanu O, Christie MR, Criger LA,
Hinderer JLM, Hollingworth RM, Johnson NS, Lantz S, Li W, Miller J, Morrison BJ, Mota-
Sanchez D, Muir A, Sepúlveda MS, Steeves T, Walter L, Westman E, Wirgin I, and Wilkie
MP (2017) Rapid evolution meets invasive species control: The potential for pesticide
resistance in sea lamprey. Canadian Journal of Fisheries and Aquatic Sciences. 75:152-
168.
23. Thompson NF, Christie MR, Marine ML, Curtis LD, Blouin MS (2016) Spawn date
explains variation in growth rate among families of hatchery reared Hood River steelhead
(Oncorhynchus mykiss). Environmental Biology of Fishes 99:581-591.
22. Christie MR, Marine ML, Fox SE, French RA, Blouin MS (2016) A single generation of
domestication heritably alters the expression of hundreds of genes. Nature Communications
7:10676.
21. Thomaz AT, Christie MR, Knowles LL (2016) The architecture of river networks can
drive the evolutionary dynamics of aquatic populations. Evolution 70:731-739.
20. Johnson DW, Christie MR, Stallings CD, Pusack TJ, Hixon MA (2015) Using post-
settlement demography to estimate larval survivorship: a coral reef fish example. Oecologia
179:729-739.
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19. Christie MR, Knowles LL (2015) Habitat corridors facilitate genetic resilience
irrespective of species dispersal abilities or population sizes. Evolutionary Applications.
18. Christie MR, Ford MJ, Blouin MS (2014) On the reproductive success of early-
generation hatchery fish in the wild. Evolutionary Applications 7: 883-896.
17. Pusack TJ, Christie MR, Johnson DW, Stallings CD, Hixon MA (2014) Spatial and
temporal patterns of larval dispersal in a coral-reef fish metapopulation: evidence of variable
reproductive success. Molecular Ecology 23: 3396-3408.
16. Fox S.E., Christie M.R., Marine M.L., Priest H.D., Mockler T.C., Blouin M.S. (2014)
De novo sequencing and characterization of the anadromous steelhead (Oncorhynchus
mykiss) transcriptome and its application for expression analyses in hatchery and wild fish.
Marine Genomics 15: 13-15.
15. Christie M.R., French R.A., Marine M.L., Blouin M.S. (2014) How much does
inbreeding contribute to the reduced fitness of captive-born individuals in the wild? Journal
of Heredity 105: 111-113.
14. Christie M.R. (2013). Bayesian parentage analysis reliably controls the number of false
assignments in natural populations. Molecular Ecology 22: 5731-5737.
13. Christie M.R., Hixon M.A. (2013) Patterns of reef-fish larval dispersal in Exuma Sound,
Bahamas in Coastal-Marine Conservation: Science and Policy (eds. G. Carleton Ray, J.
McCormick-Ray), 2nd edition.
12. Steinauer M.L., Christie M.R., Blouin M.S., Agola L.E., Mwangi I.N., Maina G.M.,
Mutuku M.W., Kinuthia J.M., Mkoji G.M., Loker E.S. (2013). Kinship analysis reveals
strong family structure in schistosome parasite samples from humans. PLoS Neglected
Tropical Diseases 7: e2456.
11. Christie M.R., Tennessen J.A., Blouin M.S. (2013) Bayesian parentage analysis with
systematic accountability of genotyping error, missing data, and false matching.
Bioinformatics 29: 725-732.
10. Christie M.R., Marine M.L., French R.A., Blouin M.S. (2012) Genetic adaptation to
captivity can occur in a single generation. Proceedings of the National Academy of Sciences
109: 238-242.
9. Christie M.R., Marine M.L., French R.A., Waples R.S., Blouin M.S. (2012) Effective size
of a wild salmonid population is greatly reduced by hatchery supplementation. Heredity 109:
254-260.
8. Carrol E., Childerhouse S.J., Christie M.R., Lavery S., Patenaude N., Alexander A.,
Constantine R., Steel D., Boren L., Baker C.S. (2012) Paternity assignment and demographic
closure in the New Zealand southern right whale. Molecular Ecology 21: 3960-3973.
7. Christie M.R., Marine M.L., Blouin M.S. (2011) Who are the missing parents?
Grandparentage analysis identifies multiple sources of gene flow. Molecular Ecology 20:
1263-1276.
Perspective by Kenyon Mobley: “Grandfathering in a new era of parentage analysis”.
Molecular Ecology 20:1080-1082.
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6. Johnson D.W., Christie M.R., Moye J., Hixon M.A. (2011) Genetic correlations between
adults and larvae in a marine fish: potential effects of fishery selection on population
replenishment. Evolutionary Applications 4: 621-633.
5. Christie M.R., Tissot B.N., Albins M.A., Beets J.P., Jia Y., Ortiz D.M., Thompson S.E.,
Hixon M.A. (2010) Larval connectivity in an effective network of marine protected areas.
PLoS ONE 5(12): e15715.
Top 1% of most cited articles in PLoS ONE
Perspective by Pete Mooreside: “Tiny larvae signal big potential for MPAs”. Frontiers in
Ecology and Evolution 9:91
Perspective by Daniel Cressey: “Plans for marine protection highlight science gap”.
Nature 469 (146):13
4. Johnson D.W., Christie M.R., Moye J. (2010) Quantifying evolutionary potential of
marine fish larvae: Heritability, selection and evolutionary constraints. Evolution 64: 2614-
2628.
3. Christie M.R., Stallings C.D., Johnson D.W., Hixon M.A. (2010) Self-recruitment and
sweepstakes reproduction amid extensive gene flow in a coral-reef fish. Molecular Ecology
19: 1042-1057.
Perspective by Dennis Hedgecock: “Determining parentage and relatedness from genetic
markers sheds light on patterns of marine larval dispersal”. Molecular Ecology 19:845-
847.
2. Christie M.R. (2010) Parentage in natural populations: novel methods to detect parent- offspring pairs in large datasets. Molecular Ecology Resources 10: 115-128.
1. Christie M.R., Eble J.A. (2009) Isolation and characterization of 23 microsatellite loci in
the yellow tang, Zebrasoma flavescens (Pisces: Acanthuridae). Molecular Ecology
Resources 9: 544-546.
3. Submitted
1. LaRue ESG, Emery NC, Briley L, Christie MR. Geographic variation in dispersal can facilitate adaptive evolution in response to climate change. Diversity and Distributions.
2. Christie MR*, Dunlop ES, Sepúlveda MS. Invasive sea lamprey may soon become resistant to their primary control agent, 3-triflouromethyl-4-nitrophenol. Evolutionary
Applications.
4. In Preparation (manuscripts available upon request)
1. Willoughby JR, Waser PM, Christie MR. Abiotic factors determine metapopulation fitness in a fully pedigreed population.
2. Martinez AS, Willoughby JR, Harder AM, Sparks M, Sepúlveda MS, Christie MR. Experimental transcriptomics uncovers incipient resistance in invasive sea lamprey.
3. Harder AM, Ardren WR, Christie MR. Within family variation in response to thiamine deficiency.
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4. Yin X, Martinez AS, Willoughby JR, Harder AM, Sparks M, Sepúlveda MS, Christie MR. Pesticide resistance genes have rapidly increased in frequency in invasive sea lamprey.
C. Invited Lectures
1. National and International Meetings
2018 Identifying physiological and transcriptional responses to 3-trifluoromethyl-4-nitrophenol
in susceptible and tolerant species (Great Lakes Fishery Commission, Cleveland, Ohio)
2017 Genomic evidence of rapid adaptation to novel environments (Redefining Darwinian
Fisheries: Integrating the Diverse Roles of Evolution in Fisheries Sustainability
Symposium, Annual Meeting of the American Fisheries Society, Tampa, Florida)
2017 The ecological and genetic sustainability of fisheries and aquaculture (The United States
Borlaug Fellows in Global Food Security program, Summer Institute for Global Food
Security, West Lafayette, Indiana)
2015 Hundreds of genes remain differentially expressed after a single generation of
domestication (Genomics of Adaptation Symposium, 145th Annual Meeting of the
American Fisheries Society, Portland, Oregon)
2015 Genetic approaches to measuring larval dispersal. The 39th larval fish conference.
(Vienna, Austria) (declined)
2015 Larval Connectivity and Local Adaptation in Yellow Perch (Great Lakes Fishery
Commission, Ann Arbor, Michigan)
2015 Assessing the chemical resistance of sea lampreys (Petromyzon marinus) to TFM (Great
Lakes Fishery Commission, Ann Arbor, MI)
2012 Pacific Coast Steelhead Management Meeting, Pacific States Marine Fisheries
Commission (Port Townsend, Washington) (declined)
2011 Larval dispersal, population connectivity and the management of marine species,
American Fisheries Society (Seattle, Washington)
2011 Assessing the role of marine protected areas in restoring, sustaining, and enhancing
fisheries, American Fisheries Society (Seattle, Washington)
2010 Where are the missing parents? Grandparentage analyses identifies reproductively
successful residualized hatchery fish. Pacific Coast Steelhead Management Meeting,
Pacific States Marine Fisheries Commission (Redmond, OR)
2010 European Society for Evolutionary Biology, 14th (Marseilles, France)
Regional Meetings and Workshops
2018 Assessing the resistance of sea lamprey to TFM (Sea Lamprey Control Board, Ann Arbor
Michigan)
2018 Genetic considerations of broodstock management (Indiana Department of Natural
Resources, Lake Monroe, Indiana)
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2016 Larval Connectivity and Local Adaptation in Lake Michigan Yellow Perch (Lake
Michigan Technical Committee Meeting, Michigan City, Indiana)
2. Universities and Other Institutions
2018 Integrating larval connectivity with local demography reveals regional dynamics of a
marine metapopulation (California Polytechnic State University, San Luis Obispo,
California).
2018 Rapid evolution in a changing world (Michigan State University, East Lansing,
Michigan).
2017 Rapid genetic adaptation to captivity causes reduced fitness in the wild (Eastern Illinois
University, Charleston, Illinois)
2016 Rapid adaptation to captivity causes reduced fitness in the wild (University of Colorado,
Boulder, Colorado)
2014 Larval dispersal, rapid adaptation, and the role of variable reproductive success (Indiana
University Purdue University Indianapolis, Indiana)
2014 Larval dispersal, rapid adaptation, and the role of variable reproductive success
(University of Southern California, California)
2014 On the role of rapid adaptation in reducing the fitness of early generation hatchery fish
(University of Oregon, Oregon)
2014 Larval dispersal and the role of variable reproductive success (Oregon Institute for
Marine Biology, University of Oregon, Oregon)
2014 Rapid adaptation and the genetics of populations (Purdue University, Indiana)
2012 Novel genetic approaches reveal patterns of dispersal and rapid adaptation (Old
Dominion University, Virginia)
2012 Genetic adaptation to novel environments can occur on ecological and evolutionary
timescales (University of Michigan, Michigan)
D. Other Presented Papers
1. National and International Meetings
2017 Genomic evidence of rapid adaptation to a novel environment. Ecological Society of
America (Portland, OR)
2013 Rapid adaptation to captivity: evidence from pedigree and gene expression data. Society
for the Study of Evolution (Snowbird, UT)
2012 Rapid adaptation to captivity can occur on ecological timescales. Ecological Society of
America (Portland, OR)
2011 Causes of fitness decline in hatchery steelhead from the Hood River. American Fisheries
Society (Seattle, WA)
2010 Where are the missing parents? Grandparentage analyses identifies reproductively
successful residualized hatchery fish. Society for the Study of Evolution (Portland, OR)
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2009 Patterns of population connectivity in a coral-reef fish. American Society of Ichthyologists
and Herpetologists (Portland, OR)
2008 Patterns of population connectivity in a coral-reef fish. Western Society of Naturalists,
(Vancouver, Canada)
2008 Larval retention and population connectivity in two coral-reef fishes. International Coral
Reef Symposium (Ft. Lauderdale, FL)
2008 Parentage in natural populations. EVO-WIBO: Evolutionary biology in the Pacific
Northwest (Port Townsend, WA)
2007 Determining patterns of larval connectivity using genetic methods. Biology Graduate
Student Symposium (Newport, OR)
2007 What determines the number of fish in the sea? National Science Board (Oregon State
University, OR)
2006 Patterns of larval retention and connectivity in a coral-reef fish. Western Society of
Naturalists (Redmond, WA)
Christie lab presentations:
2018 Harder AM, Ardren WR, Christie, MR. Impacts of thiamine deficiency on metabolic
pathways and genetic influences on disease outcomes in Atlantic salmon (American
Fisheries Society, Atlantic City, New Jersey)
2018 Martinez AS, Willoughby JR, Christie, MR. Assessing the resistance of sea lamprey
(Petromyzon marinus) to the lampricide 3-trifluromethy-4-nitrophenol (American
Fisheries Society, Atlantic City, New Jersey)
2018 Dice LM, Sparks MM, Christie MR (2018) Does Acclimatization Time Affect Response
to Lampricide Exposure in Sea Lamprey (Petromyzon marinus)?* (American Fisheries
Society, Atlantic City, New Jersey)
2017 Harder AM, Ardren WR, Christie, MR. Overview of thiamine deficiency complex and
identification of underlying genetic mechanisms (Annual Meeting of the International
Association for Great Lakes Research, Detroit, Michigan)
2017 Harder AM, Ardren WR, Christie MR. Overview of thiamine deficiency complex and
identification of underlying genetic mechanisms (Purdue University Forestry and Natural
Resources Fisheries and Aquatics Group Seminar)
2017 Martinez AM, Perkins A., Sepúlveda, MS., Christie, MR. Assessing the evolution of
resistance to lampricides in Great Lakes sea lamprey (Great Lakes Restoration Initiative -
Occurrence and Effects of Contaminants of Emerging Concern Symposium, Annual
Meeting Society of Environmental Toxicology and Chemistry North America North
America, Minneapolis, Minnesota)
2017 Willoughby JR, Tennessen JA, Scribner KT, Christie MR. Genomic evidence of rapid
adaptation to a novel environment (Annual Meeting of the Society for the Study of
Evolution, Portland, Oregon).
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2017 Willoughby JR, Christie MR. Genome-wide founder effects and rapid genetic adaptation
of Pacific steelhead to Lake Michigan (Forestry and Natural Resources Department
Seminar, Purdue).
2016 Willoughby JR, Christie MR. Captive breeding has long term demographic and genetic
effects for wild populations (Annual Meeting of the Society for the Study of Evolution,
Austin, Texas).
2016 Willoughby JR, Christie MR. Measurement of conservation need: demographic criteria
do not capture declines in genetic diversity (Ecolunch Series, Purdue).
2016 LaRue EA, Christie MR, Emery NC. Incorporating geographic variation in dispersal to
better predict a species distribution under climate change (EEB EcoLunch Series, Purdue)
2016 LaRue EA, Christie MR, Emery NC. Incorporating geographic variation in dispersal in
order to better predict a species' distribution under climate change (Annual Meeting of the
Ecological Society of America. Ft. Lauderdale, Florida)
2016 LaRue EA, Christie MR, Holland J, Emery NC. Incorporating geographic variation in
dispersal in order to better predict species' distributions under climate change (Annual
Meeting of the U.S. International Association of Landscape Ecology. Asheville, North
Carolina)
* Poster presentation; unless indicated all others were contributed talks
2. Regional Meetings and Workshops
2017 Christie MR, Genomic evidence of rapid adaptation to novel environments. Purdue Faculty
Retreat (Four Winds, Indiana)
3. Universities and Other Institutions
E. Other Professional Activities
F. Interdisciplinary Activities
G. Patents
H. Funding 1. Discussion of Support (Written by Candidate)
Since arriving at Purdue, I have received a total of $455,000 of funding in external
grant support from three separate awards. Two of the funded grants are for 3 years
of support from the Great Lakes Fisheries Commission, an international advisory
group that funds fisheries related research in the Great Lakes. The Great Lakes
Fisheries Commission has been operational since 1954 and receives continual
federal support from both Canada and the United States per the 1954 Convention
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on Great Lakes Fisheries treaty. Given the proximity of Purdue to the Great Lakes
and my lab’s ongoing research with Great Lakes fishes, I anticipate that the Great
Lakes Fisheries Commission will be a reliable source of funding for my lab. My
third grant award is an AgSeed grant that will allow our lab to collect data to
submit to aquaculture grants with larger monetary values. I currently have four
grant proposals currently under review ranging in value from $200,00 to $412,000.
Given that research in my lab spans basic and applied fields in ecology, evolution,
fisheries, and genetics, I anticipate securing funding from additional sources
including the National Oceanic and Atmospheric Administration Sea Grant
program, U.S. fish and wildlife service, and large non-profit agencies such as
Conservation International.
2. Funding
Current Awards:
1. Agency/Title of Grant: Great Lakes Fisheries Commission; Population connectivity and local adaptation in yellow perch (Perca flavescens).
2. Duration of Funding: 3 years 2018-2020 3. Total amount of award: $200,000 4. Role: Principal Investigator
co-PI Tomas O. Höök, Department of Forestry and Natural Resources
(Purdue University)
1. Agency/Title of Grant: AgSEED (Agricultural Science and Extension for Economic Development); Improving Indiana aquaculture and fisheries by
sequencing and characterizing the genome of yellow perch (Perca flavescens).
2. Duration of Funding: 1 year; 2018-2019 3. Total amount of award: $50,000 4. Your Role: Principal Investigator
1. Agency/Title of Grant: Great Lakes Fisheries Commission; Assessing the resistance of sea lampreys (Petromyzon marinus) to the lampricide TFM
2. Duration of Funding: 2016-2018 3. Total amount of award: $200,000 4. Role: Principal Investigator
co-PI Maria S. Sepúlveda, Department of Forestry and Natural Resources
(Purdue University)
1. Agency/Title of Grant: Indiana Department of Natural Resources; Assessing the genetic diversity of muskellunge (Esox masquinongy)
2. Duration of Funding: 2018-2019 3. Total amount of award: $5000 4. Role: Principal Investigator
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1. Agency/Title of Grant: National Science Foundation; Evolutionary rescue in response to infectious disease: when will populations be rescued from
pathogens?
2. Duration of Funding: 2019-2021 3. Total amount of award: $401,363 4. Role: Co-PI
Pending Awards (Under review, no award decision has been made):
1. Agency/Title of Grant: Great Lakes Fisheries Commission; Identifying the
mechanism and timing of sea lamprey resistance (Petromyzon marinus) resistance to TFM
2. Duration of Funding: 2020-2022 3. Total amount of award: $349,000 4. Role: Principal Investigator
1. Agency/Title of Grant: Great Lakes Fisheries Commission; Genetic and
phenotypic basis for fishery-induced evolution in Lake Michigan yellow perch 2. Duration of Funding: 2020-2021 3. Total amount of award: $200,000 4. Role: Co-PI
1. Agency/Title of Grant: National Science Foundation; Genetic structure and
population connectivity in coastal marine systems 2. Duration of Funding: 2020-2023 3. Total amount of award: $412,000 4. Role: Collaborative Research; Co-PI
Past Awards:
1. Agency/Title of Grant: Thompson Coral-Reef Graduate Fellowship 2. Duration of Funding: 2 years 3. Total amount of award: $12,600 4. Your Role: Principal Investigator
1. Agency/Title of Grant: Conservation International; Larval Connectivity and Fish Population Replenishment in a Network of Marine Management Areas for
Tropical Aquarium Fisheries
2. Duration of Funding: 2 years 3. Total amount of award: $54,451.00 4. Your Role: Co-Principal Investigator
I. Evidence of Involvement in Graduate Research Program
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1. Number of M.S. (1) and Ph.D. Students Graduated (1)
Elizabeth LaRue, PhD. Date graduated: 7/29/2017
Dissertation: “Geographic variation in dispersal traits of Cakile Enentula: Implications
for the evolution of species range limits”
2. Current Graduate Students (3), Post doctorates (2), and Undergraduates (3)
Current Students Degree/
Date
Entered
Past Students Date Graduated/
Date Entered
Major Professor:
Morgan Sparks Ph.D. 2017 Elizabeth LaRue Ph.D. 2017/2012
Avril Harder Ph.D. 2015 Alex Martinez M.S. 2018/2015
Claire Schraidt M.S. 2018
Chairperson, Ph.D. Examining Committee:
Trevor Vannatta (Biological Sciences)
Ph.D. 2015 Alyssa Gleichsner (Biological Sciences)
Ph.D. 2017/2012
Member, Committee:
Samarth Marthur (Biological Sciences)
Ph.D. 2016 Gina Dembski (IUPUI)
Ph.D. 2017/2013
Riley Rackliffe (FNR)
Ph.D. 2016 Jennifer Serafin (FNR)
M.S. 2017/2014
Taylor Senegal (FNR)
M.S. 2017 Laura Ploughe (Biological Sciences)
Ph.D. 2018/2013
Elizabeth Allmon (FNR)
Ph.D. 2018 Jennifer Antonides (FNR)
Ph.D. 2018/2013
Joshua Kraft (Botany and Plant Pathology)
Ph. D. 2019 Tim Malinich
(FNR)
Ph.D. 2019/2014
Present Postdoctoral Research Associates: Former Research Associates: Xiaoshen Yin Janna Willoughby
Present Undergraduates: Former Undergraduates:
Truman Shanna Newman
Helen Abigail Perkins
Lindsey Dice
Joseph Buckley Ashley Higdon
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Lab awards:
Alex Martinez:
Ross Graduate Fellowship, 2015, $24,000
Dr. P.T. Gilham Graduate Award, 2015, $3,000
Lindsey Fellowship, 2017, $1,000
Morgan Sparks:
Frederick N Andrews Assistantship, 2017-2018, $48,000
Rosenberg Graduate Award, 2017, $4,000
Dr. P.T. Gilham Graduate Award, 2017, $3,000
Janna Willoughby:
Postdoctoral Scholar Fellowship, FNR Investments in Excellence Program, 2017-2018, $100,000
Graduate School Travel Grants, 2016-2017, $1400.
Avril Harder,
Graduate School Summer Research Grant, Purdue University, 2017, $3300
Robert Ricklefs Travel Award, Purdue University, 2017, $500
Alton A. Lindsey Graduate Fellowship in Ecology, 2016, Purdue University, $1000
Elizabeth LaRue,
Purdue Research Foundation Research Grant, 2016, $22,000
IV. ENGAGEMENT
A. Discussion of Service I have reviewed manuscripts for 26 journals. Additionally, I actively seek outreach
opportunities to engage with K-12 students and the public to share my work.
B. Department EEB critical review convener 2017-2018
PRF graduate student awards committee 2015-2016
Undergraduate Honors Student Committee 2015-2018
EcoLunch seminar organizer 2015
Umbarger Review 2017
Biological Sciences Focus Day 2017
C. College of Science Joined faculty of Computational Life Sciences 2015
Reviewer for Lynn Fellowships (Computational Life Sciences) 2016
FNR postdoctoral scholar review committee 2017
D. University
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E. Professional
1. Grant review (see below)
2. Editorial board
3. Reviewed Manuscripts for the following journals (include number of accepted requests).
Behavioral Ecology and Sociobiology (1), Bioinformatics (3), BMC Evolutionary Biology
(1), Bulletin of Marine Science (1), Canadian Journal of Fisheries and Aquatic Sciences (5),
Diversity and Distributions (1), Ecology (5), Ecology and Evolution (1), Environmental
Biology of Fishes (2), Evolutionary Applications (8), Functional Ecology (1), Heredity (5),
Journal of Applied Ecology (2), Journal of Heredity (1), Journal of Marine Biology (1),
Journal of Theoretical Biology (1), Marine and Freshwater Research (1), Marine Ecology
Progress Series (8), Methods in Ecology and Evolution (1), Molecular Ecology (22),
Molecular Ecology Resources (7), Nature Communications (2), Nature Ecology & Evolution
(3), PeerJ (1), Proceedings of the National Academy of Sciences USA (4), PLoS Biology (2),
PLoS One (3), Reviews in Fish Biology and Fisheries (1), Science (1), Science Advances (1),
Transactions of the American Fisheries Society (2).
Books: Evolutionary Ecology of Marine Invertebrate Larvae, Oxford Press, (eds Carrier,
Reitzel & Heyland).
4. Reviewed Grants for the following agencies (include number of requests) National Science Foundation (8), Alaska Sea Grant (1), National Oceanic and
Atmospheric Administration (3), National Geographic Society, Icelandic Research Fund,
Oregon Department of Fish & Wildlife, Washington Department of Fish & Wildlife
Contacted and participated on Grant Panels by a state or federal representative
NSF DEB (Arlington, VA) 2016
F. Diversity Activities
G. Other Engagement Activities
Outreach and Media:
2018 Outreach publication in The Osprey, an angler-supported journal of salmon and steelhead
conservation:
Harder, AMG, Willoughyby JRP (2018) Great Lakes steelhead win the adaptation lottery.
The Osprey 91: 19-21
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2018 Additional coverage of Willoughby et al. 2018: McCallum E (2018) A fish out of salt
water. Journal of Experimental Biology. 221:3-4.
2015 Regular contributor to the “Molecular Ecologist”, the web log of Molecular Ecology
Posts available at: http://www.molecularecologist.com/author/mark-christie/
2012 Lecture and Q&A for Tri Beta Biology Honor Society, Georgia Institute of Technology
2012 Christie et al. 2012 (PNAS) was covered by the Associated Press, NPR, The Oregonian,
The New York Times, and other media outlets. Science daily article titled “Hatcheries
change salmon genetics after a single generation.” It was also reviewed by Faculty of
1000.
2012 Carrol, Childerhouse, Christie et al. 2012 (Molecular Ecology) was covered in Science
Daily and other news organization. Science daily article titled “First paternity study of
southern right whales finds local fathers most successful.”
2011 Interviewed for National Public Radio (NPR). Available at:
http://earthfix.opb.org/water/article/taming-the-wolves-new-research-shows-hatchery-
fish/
2011 Lecture and Q&A session to Trout Unlimited, Eugene Oregon chapter
2011 Outreach publication in The Osprey, an angler-supported journal of salmon and steelhead
conservation:
Christie M.R., McMillan J.R. (2011) Steelhead and resident rainbow relationship slowly
revealed. The Osprey 69: 11-13.
2011 Christie et al. 2011 (Molecular Ecology) was reviewed by K. Mobley in “News and
Views” column of Molecular Ecology (2011) 20: 1080-1082 and featured in Audubon
2010 Developed and implemented activities for the workshop, “Darwin’s legacy: modern
explorations of evolutionary biology,” a program for local high school students preceding
a lecture by Peter and Rosemary Grant. Corvallis, Oregon.
2010 Christie et al. 2010 (PLoS ONE) was reviewed in "News" column of Nature (13 Jan
2011) 469:146, reviewed in “Dispatches” column of Frontiers in Ecology and the
Environment: (2010) 9(2): 91 and was also reviewed by Faculty of 1000.
2010 Invited speaker on “Oregon Outdoors” radio show
2006-2009 National Ocean Science Bowl: Salmon Bowl Science Judge
2005-2007 Evolutionary biology blog co-founder/contributor
V. Mentoring Mentoring is an essential component of my lab. Since arriving at Purdue University, I have
mentored 7 undergraduate students in research, 4 graduate students, and 2 postdoctoral
researchers. All of these students are currently or have conducted independent projects in my lab.
One undergraduate student completed her honors thesis by examining the role of oxygen
consumption in sea lamprey exposed to the lampricide TFM; these data are included in a
manuscript that is currently in preparation. Two undergraduates are currently quantifying genetic
diversity in Indiana Muskellunge (Esox masquinongy) and we will be presenting our findings to
http://www.molecularecologist.com/author/mark-christie/http://earthfix.opb.org/water/article/taming-the-wolves-new-research-shows-hatchery-fish/http://earthfix.opb.org/water/article/taming-the-wolves-new-research-shows-hatchery-fish/
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the Indiana Department of Natural Resources in the Spring. I expect that one of the two younger
undergraduates will also pursue an honors thesis. I currently have 3 graduate students a