Budding or Anagenesis? Paraphyly and

Ancestor-Descendant Relationships from Tip-Dating Phylogenies of

Fossil Lineages

David Bapst & Sandra Carlson

University of California Davis

Evolution 2017 Portland

Sunday, June 25th Feel free to

tweet this talk!

@dwbapst

The Question of Ancestors in the Fossil Record

Fortey and Cooper 1986

Morphotaxa inthe Fossil Record

• Often, we find specimens of varying age with similar morphology

• We use those features to define morphotaxaspanning geologic time

Dicellograptus

• Interpret occurrences as a chain of direct ancestor-descendant relationships

• Central assumption since the dawn of paleontology, critical to biostratigraphy

… and rarely testedDicellograptus

The Most Fundamental Assumption in Paleontology?

Maletz & Mitchell (1996)

Qualitative Interpretations of Ancestor-Descendant Relationships

Among Morphotaxa

Kennett and Srinivasan (1983) from Pearson (1998)

May Read the Fossil Record Too Literally

The problem is, very rarely can we read the fossil record as literally as this

How do we infer the relationships among ancestors & their descendants,

given the incompletenessof the fossil record?

Stratocladistic Methods Attempted To Make This More Rigorous

Bloch et al., 2001• Treated implied gaps in the fossil record as interchangeable with character changes under maximum parsimony (Fisher, 1991; 1994)

Bayesian sampled-ancestor tip-dating• Infer dated phylogenies under a model of morph

character change, and under a formal model of diversification and incompleteness of rock record: the Fossilized Birth-Death Model (Heath et al., 2014)

• Taxa, as point occurrences in time, potentially placed as sampled-ancestors (Gavryushkina et al., 2014)

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In The Age Of Ancestor Inference…

Beast2(PP)

MrBayes(PP)

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• Different methods agree on placing ancestors [dinosaurs]

• Quantitative inferences agree with previous putative pairs of ancestor-descendants [trilobites]

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Static Morphotaxa vs. Points in Time• Morphotaxa in most fossil-rich groups are not

point occurrences in time (even many dinosaurs have stratigraphic durations)• Most studies have treated taxa with durations as a single

occurrence in time, usually earliest (first) occurrence

• Despite FBD assuming every sampled occurrence counted

• What happens with datasets where individual occurrences are the operational taxon units?

• What happens if we treat individual morphotaxa as multiple operational taxon units?

Allow us to test for a range of ancestral relationships

Anagenesis

‘Budding’ Cladogenesis

Previous analyses find more evidencefor budding (Wagner & Erwin, 1995; Bapst & Hopkins, 2017)

No new morphotypes without branching?

Asymmetry of cladogenetic change?

‘Budding’ Cladogenesis

Anagenesis

Budding evidenced by paraphyly of occurrences assigned to same morphotaxon

‘Budding’Anagenesis

Notice that budding can look like anagenesis (but not vice versa)

in an incomplete record

Individual Occurrences as Operational Taxon Units

Hunt, 2007

20 Poseidonomicus species

Time (Mya)

Tip-Dating Ostracod Occurrences

3 previously defined morphospecies are paraphyletic (budding!)

12 sampled ancestors

Bapst, in prep.

Tip-Dating with First and Last Occurrences

• A kludge: Duplicate character data for each taxon, put separate uniform age priors for first and last occurrences • thus doubling the number of tips

• Genus-level analyses for three groups of mid-Paleozoic brachiopods: Terebratulides, Pentamerides, and Stenoscismatoids (Carlson & Fitzgerald, 2008; Carlson, unpub.)

• Wrote R functions for automating and streamlining creating NEXUS files with MrBayes blocks for tip-dating, including analyses with empty matrices and topological constraints

• https://github.com/dwbapst/paleotree

Outgroups

MCCT

MCCT for Devonian Terebratulides

• 9 paraphyletic genera among 72

• 21 sampled anc. (all first occs. ancestral to last)

How does this vary across the posterior?

10-50% of OTUs as Sampled Ancestors

Values Across the Post-Burnin Posteriors

Terebr: 67 char, 78 genPentam: 65 char, 84 genSteno: 30 char, 26 gen Bapst & Carlson, in prep.

About 25% of SA are Last Occurrences: 10-22% Upper Limit on Anagenesis

Terebr: 67 char, 78 genPentam: 65 char, 84 genSteno: 30 char, 26 gen Bapst & Carlson, in prep.

Majority of SA are First Occ. As Ancestors to Last Occ. (Especially in Pentamerides)

Terebr: 67 char, 78 genPentam: 65 char, 84 genSteno: 30 char, 26 gen Bapst & Carlson, in prep.

Budding (Paraphyletic Taxa) 2-4x More Common Among Terebratulides and Stenoscismatoids

Terebr: 67 char, 78 genPentam: 65 char, 84 genSteno: 30 char, 26 gen Bapst & Carlson, in prep.

A New Era of Ancestors on Trees• Treating fossil morphotaxa as more than single OTUs sheds

light on patterns of ancestor-descendant relationships

• Earliest occurrences are frequently sampled ancestors to their last occurrence, reaffirming that morphotaxa are often ancestor-descendant sequences (but maybe not always)

• Budding likely more common than anagenesis: 10-22% of last occ. as SA (= maximum anagenesis), but paraphyletic taxa mostly as common (= minimum budding)

• Ancestor-descendant relationships varied in pattern (esp. Pentam. vs other groups)

This research was funded by NSF grant EAR-1147537.

Thanks for listening! Questions?

Gaps in Densely-Sampled Fossil Records

Maletz and Zhang, 2003; Vandenberg, 2003; C.E. Mitchell

• Closest relatives separated by a 15 to 20 million year gap in this lineage:

• Were the intermediates living somewhere else? Open ocean?

BergstromgraptusMiddle Darrwillian

SinoretiograptusLatest Katian

The Question of Ancestors in the Fossil Record

?

Tip-Dating with Mesozoic Theropods• We used a somewhat infamous dataset to compare

tip-dating methods with cal3, for ancestor-descendant relationships, divergence dating, estimating evolutionary rates, etc...• Do the methods agree?

• The support for particular taxa to be probable ancestors were fairly correlated across methods

• So… Is Archaeopteryx really the ancestral bird?

Bapst, Wright, Matzke & Lloyd, 2016; Biol. Lett.2. Ancestor-Descendants in the Fossil Record

withApril Wright Graeme LloydNick Matzke

• Significant rank-order pair-wise correlations of ancestral placement between methods• Strongest between MrBayes

and BEAST2

• Considerable differences despite similar model

• Median # of ancestors per tree for tip-dating = 1-2

• With cal3 (using entire taxon durations) = 17• Always buddingBeast2

(PP)MrBayes(PP)

cal3(prop)

Bapst, Wright, Matzke & Lloyd, 2016

Whither the Ancestral Bird?

• Archaeopteryx rarely placed as a sampled ancestor

• Never placed as ancestor on lineage leading to extant birds, but rather as a sampled ancestor to itssister taxon / possible synonym Wellnhoferia

Bapst, Wright, Matzke & Lloyd, 2016

Case 1: Cambrian pterocephaliid trilobites

• Hopkins (2011) did a cladistic analysis and reviewed a number of (qualitative) ancestor-descendant pairs previously suggested for this group

• Does cal3 find support for those pairs, and does it match the mode inferred by previous authors?• Apply cal3 to the single maximum-parsimony topology &

100 CONOP solutions from Hopkins (2011)

• Obtained 100 dated phylogenies, quantified support for a given AD pair as the proportion of trees

Bapst & Hopkins, now in press at Paleobiology!

Each pair is a stacked barplot

Dots indicate putative pairs

Evidence for alla priori AD pairs, & a few extra

cal3 finds very little support for anagenesisGiven biases,

perhaps entirely budding?

• Each pair is a stacked barplot

• Dots indicate putative pairs

• Support for alla priori AD pairs, & a few extra

• cal3 finds very little support for anagenesis

• Support for budding suggests globally instantaneous origins of new morphotaxa

2. Ancestor-Descendants in the Fossil Record