temperature-induced shifts in selective pressure at a critical developmental transition
TRANSCRIPT
Oecologia (2007) 152:219–225
DOI 10.1007/s00442-006-0647-1POPULATION ECOLOGY
Temperature-induced shifts in selective pressure at a critical developmental transition
Monica Gagliano · Mark I. McCormick · Mark G. Meekan
Received: 3 August 2006 / Accepted: 11 December 2006 / Published online: 23 January 2007© Springer-Verlag 2007
Abstract Selective mortality within a population,based on the phenotype of individuals, is the founda-tion of the theory of natural selection. We examinedtemperature-induced shifts in the relationships amongearly life history traits and survivorship over theembryonic and larval stages of a tropical damselWsh,Pomacentrus amboinensis. Our experiments show thattemperature determines the intensity of selective mor-tality, and that this changes with ontogeny. The size ofenergy stores determined survival through to hatching,after which egg size became a good indicator of Wtnessas predicted by theoretical models. Yet, the beneWtsassociated with egg size were not uniform among testtemperatures. Initial egg size positively inXuenced lar-val survival at control temperature (29 °C). However,this embryonic trait had no eVect on post-hatching lon-gevity of individuals reared at the higher (31 °C) andlower (25 °C) end of the temperature range. Overall,our Wndings indicate that the outcome of selective mor-tality is strongly dependent on the interaction betweenenvironment conditions and intrinsic developmentalschedules.
Keywords Bigger is better hypothesis · Early life history traits · Egg size · Selective mortality · Coral reef Wsh
Introduction
Variation in life history traits leads to variation in sur-vival among individuals (Stearns 1992). Life historytraits are aVected by physiological, ecological andbehavioural regimes that diVerentially inXuence earlysurvival and which individuals ultimately enter adultpopulations. Because individuals are generally poorlydeveloped, relatively small and limited in their abilityto avoid predation at birth, and they often experiencestarvation and transport to detrimental habitats, mostorganisms experience high mortality rates during theearly phases of their lives (RoV 1992). These early mor-tality rates are particularly high in marine teleostWshes, where mortality has been estimated to be near100% (Bradford and Cabana 1997). Although theembryonic and larval periods account for only a smallproportion of the total life span of a Wsh, very smallchanges in selective mortality during these crucialontogenetic periods can have far greater repercussionson population Xuctuations than changes occurring inlater life stages (Houde 1987; Pepin and Myers 1991;Cushing and Horwood 1994).
A wide range of extrinsic variables, both abiotic (e.g.salinity, oxygen, light, pH) and biotic (e.g. food avail-ability, social organization), interact with the develop-mental program of an individual to inXuence theexpression of its early life history traits. Of these, tem-perature is undoubtedly among the most important forectotherm ontogeny because of its pervasive eVects on
Communicated by Martin Attrill.
M. Gagliano (&) · M. I. McCormickAustralian Research Council Centre of Excellence for Coral Reef Studies, School of Marine and Tropical Biology, James Cook University, Townsville, QLD 4811, Australiae-mail: [email protected]
M. G. MeekanAustralian Institute of Marine Science, Building 42, Northern Territory University, Darwin, NT 0909, Australia
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biological rate processes, altering nearly all physiologi-cal functions (Johnston and Bennett 1996). In cross-taxonomic analyses, temperature alone has beenreported to account for over 50% of the variability inearly survival (Houde 1989). In teleosts there is abun-dant evidence that temperature has a profound eVecton life history traits through its inXuence on develop-ment and growth, and consequently physiological andbehavioural capabilities (Koumoundouros et al. 2001).Since the most substantial morphological, physiologi-cal and behavioural changes occur almost exclusivelyover the relatively short period of embryonic and larvallife (Fuiman and Higgs 1997), temperature can be con-sidered a major agent driving the large variation intraits during the early life history of Wsh. Yet, patternsof temperature-mediated plasticity are complex andtheir importance in shaping adaptive responses at thepopulation level of many organisms remains diYcult topredict (Stillwell and Fox 2005).
Because Wsh ontogeny is a multiplicative processthat proceeds continuously with temporary accelera-tions (Kamler 2002), selective processes in the larvalphase are expected to act on the collection of changesderived from the embryonic phase and inXuence thephenotypic characteristics of those surviving. Egg sizeis certainly one of the most intensely studied early lifehistory traits of Wshes, and variation in this trait and itsconsequences for survival have been documentedextensively, particularly in temperate systems (e.g.Chambers et al. 1989; Bernardo 1996; Johnston andLeggett 2002). Larger eggs appear to confer higher sur-vival to oVspring than smaller ones, because they com-monly generate larger larvae at hatching (e.g. McGurk1986). Ultimately, larger larvae are expected to be bet-ter at food capture, more resistant to starvation, andless susceptible to predators (the “bigger is better”hypothesis, Miller et al. 1988).
Despite the widespread acceptance of the “bigger isbetter” paradigm, there is also evidence that does notsupport it (e.g. Litvak and Leggett 1992; Leggett andDeBlois 1994; Lankford et al. 2001; Green and Fisher2004). Indeed, Wtness consequences of egg size variabil-ity can change dramatically among environments suchthat selection may favour diVerent size eggs underdiVerent environmental conditions (e.g. Einum andFleming 1999), or its inXuence may not be revealedwhen the object of selection is a correlated trait(Einum and Fleming 2000). Yet, little is known aboutthe inXuence of environmental conditions on embry-onic trait interrelationships and how ontogeneticchanges in the relationship among early life historytraits aVect survival during and immediately after theembryonic stage. We therefore set out to experimentally
test the generality of the “bigger is better” hypothesisby investigating the interrelationships of life historytraits at the individual level for a tropical damselWsh(Pomacentrus amboinensis), from fertilization to theexhaustion of endogenous nutritional reserves. Weexamined the extent to which variation in oVspring sur-vival may be inXuenced by individual phenotypic char-acteristics, and investigated temperature-induced shiftsin trait association and survival. P. amboinensis is agood model organism for studying the factors inXuenc-ing trait interrelationships because the species displaysconsiderable variation in a number of early life historytraits (McCormick 1999).
Materials and methods
Experimental animals
Egg clutches used in this experiment were collected inlate December 2003 at one location on the fringing reefat Lizard Island, Great Barrier Reef (14° 40� S, 145°28� E). Three clutches of newly fertilized eggs spawnedon artiWcial nesting substrata (McCormick 1999) wereobtained in the morning following a pre-dawn spawn-ing and transferred into well-aerated Xow-through sys-tem aquaria in the laboratory. Eggs were removedfrom each clutch using a scalpel and individualembryos were transferred with a Wne brush to 16 mlwells of six-well tissue culture plates. Plates wereplaced in perforated seawater baths and submerged(»4 cm deep) with a surface Xow of aerated seawater(3 § 0.4 l h¡1) to maintain high oxygen levels aroundthe negatively buoyant eggs and to minimize potentialbacterial infections. Embryos were taken from twopositions in the clutch, periphery (within 1 cm of theedge) and centre, to account for the potential variabil-ity associated with the position of the egg within aclutch. In total, 216 embryos from all clutches wererandomly apportioned among all three temperaturetreatments (25, 29 and 31 °C) to account for the poten-tial eVect of variability among clutches. Embryos weremaintained individually throughout the study andallowed to develop in isolation at the three diVerenttemperatures in two replicate plates. The 29 °C tem-perature group was referred to as the control treat-ment, being held at the same seawater temperaturerecorded on the reef where the clutches were collected.The 25 and 31 °C temperature groups were referred toas the cold and hot treatments respectively. The coldand hot treatments were obtained by using headertanks with chillers and heating units, respectively.These temperatures were chosen to represent the
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realistic temperature range on the northern Great Bar-rier Reef during the entire breeding season.
Embryonic traits and survival
To deWne the extent to which temperature may inXu-ence the expression of early life history traits prior tohatching and subsequent survival of oVspring, embryosfrom the three temperature treatments were moni-tored during their development at 36 and 84 h post-fertilization (hpf). Key criteria used to measure thedevelopmental stage of P. amboinensis embryos werethe presence of a rudimentary heart at 36 hpf andthe complete development of the arteria caudalis to theend of the notochord at 84 hpf (McCormick andNechaev 2002). Based on these criteria, all embryosthat survived to the Wxed observation times (i.e., 36 and84 hpf) were assessed to be at a comparable develop-mental stage among the three incubation tempera-tures.
The dorsal side of each individual embryo was pho-tographed under a compound microscope (10£ magni-Wcation) at 36 and 84 hpf, and egg size (maximum egglength, mm), yolk-sac size (yolk-sac area, mm2) and oilglobule size (oil globule area, mm2) were measuredfrom these calibrated digital images using the imageanalysis programme OPTIMAS 6.5 (OPTIMAS Cor-poration). Heart rates (heart beats/min) were mea-sured by three replicated 1-min counts of heart beats at84 hpf and used as a proxy for metabolism. Pre-hatch-ing mortality and time of hatching were recorded. Fol-lowing hatching, unfed larvae were inspected every12 h until death as a measure of post-hatching longev-ity based only on pre-existing reserves. IndividualdiVerences in post-hatching longevity were measuredas a realistic representation of relative diVerences intime available (and opportunity) to encounter suitablefood before irreversible starvation in the wild. Limitedfood availability may be a realistic condition in thepelagic environment of tropical waters, as food avail-ability is notoriously limited and patchy at both tempo-ral and spatial scales and starvation is implicated as oneof the major sources of mortality in Wsh larvae (Kerri-gan 1997).
Statistical analyses
Prior to analysis, longevity measures were square-root-transformed to meet the assumptions of normality andhomogeneity of variance, allowing parametric tests ofsigniWcance. The eVect of temperature, clutch identityand position of origin within the clutch on pre- andpost-hatching longevity were analysed using repeated-
measures analysis of variance (ANOVA), with time(number of hours at death) as the within-subjects fac-tor and temperature treatments (25, 29 and 31 °C),clutch identity and position of origin (centre andperiphery) as between-subjects factors. DiVerencesamong temperature treatments, between clutches andbetween positions were identiWed using a post hocTukey honestly signiWcant diVerence (HSD) test at asigniWcance level of 0.05/k, where k is the number ofsampling times (k = 2). The eVect of time to hatch onpost-hatching longevity among temperature groupsand within a temperature group was tested by one-wayANOVA and t-test respectively.
To measure the eVect of selective mortality on aphenotypic embryonic characteristic prior to and afterhatching, partial regression coeYcients of longevity onthe phenotypic traits were calculated as described inLande and Arnold (1983). Phenotypic selection gradi-ents (�) representing the change in mean value of aphenotypic trait due to selective mortality were stan-dardized (��) by the standard deviation units of eachtrait, except for survival. Prior to the multiple regres-sion analysis, the assumption of no collinearity of theindependent variables was met by examining the levelsof correlation among traits.
Results
Mortality occurred prior to and after hatching. Clutchidentity and position within the clutch had no inXuenceon survival prior to or after hatching (clutch identity:F(2,155) = 2.679, P = 0.072; position within the clutch:F(1,155) = 0.466, P = 0.496). However, pre- and post-hatching mortality were strongly dependent on tem-perature treatment (F(2,155) = 26.773, P < 0.001). Sur-vival prior to hatching was signiWcantly compromisedat high temperatures (31 °C), where mortality was 3.6times higher than in the cold temperature treatment(Tukey HSD, P < 0.001) and accounted for over 54%of all mortality occurring prior to hatching across tem-perature treatments. After hatching, larval longevity inthe high temperature treatment was also signiWcantlyreduced with hatchlings surviving no longer than 36 h.Embryos developing at 25 and 29 °C had similar sur-vival rates prior to and following hatching (TukeyHSD, P = 0.699).
Eighty percent of all eggs hatched at about 85 h post-fertilization, regardless of the temperature at whichthey were incubated. The remainder hatched a day later(i.e. 108 hpf) and had all been incubated at 25 °C.Despite these diVerences in hatching time, time to hatch(85 vs. 108 hpf) had no signiWcant eVect on post-hatching
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longevity overall (F(1,97) = 0.6364, P = 0.427), or withinthe 25 °C group (t41 = ¡0.38, P = 0.709).
Initial yolk-sac area was the only trait that covariedwith pre-hatching survival. In the highest temperaturetreatment, rate of survival was higher amongstembryos with larger initial yolk-sac area than thosewith smaller yolk sacs (F(1,50) = 26.12, P < 0.001, Fig 1).No selective mortality based on yolk-sac area wasdetected for embryos reared at 25 and 29 °C. The eVectof yolk-sac size on survivorship disappeared afterhatching. Initial egg size and heart rate aVected post-hatching longevity at speciWc temperatures (egg size at29 °C: F(2,114) = 3.375, P < 0.001; heart rate at 31 °C:F(2,114) = 2.230, P < 0.05, Fig. 2). An examination ofphenotypic selection gradients, using longevity as ameasure of Wtness, found a clear trend for the survivalof individuals that displayed larger initial egg size andhigher heart rates at 84 hpf. However, no signiWcantcorrelation was observed between the two traits (25 °Cgroup: r = ¡0.065, P = 0.714; 29 °C group: r = 0.005,P = 0.969; 31 °C group: r = 0.336, P = 0.118), and phe-notypic selection gradients indicated that selectivemortality operating on initial egg size was intense onindividuals in the 29 °C group exclusively, while selec-tive pressure against individuals that had a low heartrate at 84 hpf was only experienced by larvae in the31 °C group. No selective mortality was observed inindividuals kept at 25 °C (Table 1).
Discussion
By examining temperature-induced shifts in selectivemortality in P. amboinensis, the present study high-lights the profound eVects of temperature on an indi-vidual’s viability during the early life stages of tropicalWshes. Although the generality of the present study islimited by the restricted number of clutches fromwhich eggs were collected, the study does have somebroad-reaching implications. To our knowledge, this isthe Wrst study to explore the interrelationships amongearly life history traits at the level of the individual fora tropical reef Wsh and relate these to early survival.Here, we demonstrate changes in intensity of pheno-typic selection on these traits in response to tempera-ture variations and between ontogenetic stages.
Initial yolk-sac size was important for embryo sur-vival to hatching at the high temperature but had nosigniWcant eVect on initial survival for embryos rearedat control or lower temperatures. This suggests thatwhether phenotypic selection alters the distribution of
Fig. 1 Mean yolk-sac area (mm2) of P. amboinensis embryos thatdied before hatching (black bars) and embryos that survived tohatch (white bars) at low (25 °C), control (29 °C) and high (31 °C)incubation temperature. Error bars are 95% conWdence intervals.n.s. no signiWcant diVerence; **signiWcant diVerence at � = 0.025
0.15
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0.19
0.21
0.23
0.25
low control hightreatments
mea
n yo
lk-s
ac a
rea
(mm
2 )
n.s.n.s.
**
Fig. 2a–b Longevity of larval P. amboinensis in relation to (a)initial egg size (mm) at 29 °C and (b) heart rate (beats min¡1) at31 °C recorded at approximately 84 h post-fertilization. Errorbars are 95% conWdence intervals
175
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185
190
195
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205
hear
t rat
e (b
eats
min
-1)
(b)
1.22
1.24
1.26
1.28
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1.32
0
egg
size
(m
m)
(a)
longevity (hrs)<12 <7224 48 72
0
longevity (hrs)
<12 7224 48
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this trait or not depends on the environmental condi-tions to which individuals are exposed (Lynch andGabriel 1987). Given that the yolk sac contains theonly nutritional reserves available to the embryo for itsdevelopment, embryos with larger yolk sacs havehigher probabilities of growth and survival, at least upuntil hatching. Temperature is known to directly inXu-ence the rate and eYciency with which yolk is con-verted into tissue (Blaxter 1988), and yolk is depletedmore rapidly as temperature rises throughout therange of thermal tolerance (Collins and Nelson 1993).Temperature extremes have been found to limit therange of normal embryonic development by aVectingprotein and fat metabolism at upper and lowerextremes respectively (Ehrlich and Muszynski 1982).Thus, elevated temperature may operate directly onthe rate and eYciency of yolk absorption by alteringprocesses associated with yolk protein metabolism.
Interestingly, we observed no ramiWcations of yolk-sac size on embryonic success to hatching at ambientand low temperatures. This may be because low tem-peratures principally aVect lipid metabolism (Ehrlichand Muszynski 1982), which is relatively unimportantuntil after hatching, when activity and energy require-ments increase (Heming and Buddington 1988). Over-all, evidence suggests that P. amboinensis embryos areprovisioned with suYcient yolk to survive the range oftemperatures they would naturally encounter at thestudy location, but they have reduced ability to com-pensate metabolically for the eVects of temperatures atthe high end of their range.
Yolk-sac size was not related to post-hatching lon-gevity, indicating a shift in the importance of this trait
with ontogeny. The lack of relationship between initialyolk-sac size and post-hatching longevity agrees withprevious Wndings in temperate Wsh (Chambers et al.1989). However, it diverges from conventional general-izations (Blaxter 1988) by suggesting that an initiallylarger amount of yolk reserves does not directly lead tohatchlings that survive longer before irreversible star-vation. During the embryonic phase the yolk sac servesas a primary nutrient reserve and the delivery rate ofsuch nutrients through the circulatory system is deter-mined by variable developmental rhythms and periodicaccelerations in tissue growth (McCormick andNechaev 2002). As yolk utilization is inXuenced byvariable metabolic rates throughout the egg stage, yolkreserves at hatching rather than at the beginning ofembryonic development are more likely to aVect post-hatching longevity. Unfortunately, yolk-sac size athatching could not be measured in the present study.
Post-hatching longevity was aVected by initial eggsize and pre-hatch embryonic heart rate. In the hightemperature treatment in particular, post-hatching lon-gevity was positively aVected by heart rate just prior tohatching. Heart rate is closely dependent on incubationtemperature and the ontogenetic stage of the embryo.Shortly before hatching, the chorion is softened anddissolved by a hatching enzyme and increased embry-onic activity assists in breaking through the egg enve-lope (Yamagami 1988). In P. amboinensis, theenhanced activity of the embryo at the start of choriondissolution and consequently the raised energeticdemands are associated with an increase in heart rate(McCormick and Nechaev 2002). At higher tempera-ture, the dissolution of the egg envelope by enzymaticaction occurs more quickly (Yamagami 1988), heartrate increases further and embryonic movementsbecome more rapid (Klinkhardt et al. 1987). The pres-ent Wndings suggest that slow heart rate may be an indi-cator of reduced physiological viability. In contrast,individuals with higher metabolism may be moreeYcient at utilizing yolk reserves and mobilizing addi-tional nutrients from the dissolution of the chorion.Individuals with higher metabolism have been shownto have a greater capacity for energetically expensiveactivities in salmonids (Metcalfe et al. 1995). Conse-quently, despite a cost associated with elevated energydemand, higher metabolic rate may be advantageouswhen translated into higher metabolic scope and con-sequently greater potential for fast growth (Priede1985).
Despite the assumption that selection favours largeregg size over a wide range of taxa (reviewed by RoV1992), the present experiment found that initial eggsize positively inXuenced larval survival only at
Table 1 Phenotypic selection gradients (� § SE) for initial eggsize (maximum egg length, mm) and metabolic rate (heart beatsper min), using post-hatching longevity of P. amboinensis larvaefrom three temperature groups as a measure of Wtness
Temperature groups (25, 29 and 31 °C) corresponded to the nat-ural temperature range recorded on the northern Great BarrierReef during breeding seasons. Standardized selection gradients(��) are in standard deviation units. r2 values are for the multipleregression; P < 0.05 in bold
Post-hatching longevity
� § SE �� § SE r2 P
Low temperature (25 °C)Initial egg size 12.77 § 11.88 0.19 § 0.18 0.05 0.291 Heart beat rate 0.02 § 0.03 0.11 § 0.17 0.521Control temperature (29 °C)Initial egg size 18.01 § 6.90 0.33 § 0.09 0.11 0.030Heart beat rate 0.01 § 0.01 0.01 § 0.12 0.348High temperature (31 °C)Initial egg size 20.23 § 16.50 0.23 § 0.19 0.37 0.235Heart beat rate 0.04 § 0.01 0.49 § 0.18 0.017
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ambient temperatures. In a recent study, Gaglianoand McCormick (2007) showed that P. amboinensisfemales produce a broad range of egg sizes within andamong clutches, and this may be a means of spreadingthe mortality risk of oVspring in case unfavourableenvironmental conditions are encountered throughoutdevelopment (i.e. bet-hedging, Philippi and Seger1989). While there is little doubt that propagule size iscorrelated with oVspring Wtness, the present studyshowed that the magnitudes of size-related eVects onlongevity depend strongly on the thermal environment.We found no eVect of initial egg size on post-hatchinglongevity at high and low temperatures, suggesting thatbeneWts associated with initially larger egg size canshift or even disappear in response to the thermal envi-ronment. Some characteristics of the oVspring environ-ment can directly inXuence the optimal egg size in Wsh(Hutchings 1991; Einum and Fleming 1999, 2002), sug-gesting that temperature-induced shifts in trait optimamay not be rare (Norry and Loeschcke 2002). Thus,because egg size does not appear to be advantageous atall points in development and under all circumstances(e.g. discrete stages model, Hendry et al. 2001), theheterogeneity of developmental opportunities imposedby temperature conditions might be one reason why wedo not see a continual evolution towards an increas-ingly large egg size.
This study has demonstrated that environmentalconditions under which P. amboinensis embryosdevelop and hatch have a great inXuence on their post-hatching life. Besides generating a marked reduction inthe variability of phenotypic characteristics of individu-als, water temperature during early development ofP. amboinensis embryos caused signiWcant changes inmetabolic processes. In particular, elevated tempera-ture was found to directly alter processes associatedwith yolk protein metabolism during the embryonicphase and also to aVect individual larval viabilitythrough higher heart rates. While the present resultsmay only be applicable to this particular set of environ-mental parameters, similar patterns of plasticity in theexpression of metabolic activity are common, and theprofound eVects of temperature on an individual’sdevelopmental physiology are widespread (see meta-bolic theory, Brown et al. 2004).
Although the current experiment cannot distinguishbetween behavioural choices of parents to maximizematernal Wtness and those that may maximize oVspringWtness, several lines of reasoning suggest some form ofadaptation to local environmental conditions that max-imizes embryonic survival rates. Nonetheless, the con-ditions under which embryonic development occursare ultimately dependent on parental choice. The
capacity of parents to alter their environment in a waythat alleviates the negative eVects of unfavourableenvironmental conditions may also increase oVspringsurvival and Wtness later in life (Clutton-Brock 1991).In several Wsh species, parental activities such as nestbuilding, cleaning, fanning, brooding, guarding, andeven cannibalizing their own eggs have been shown toat least partly mitigate the negative repercussions ofunusually stressful physical environments (e.g. Payneet al. 2002; Green and McCormick 2005; Kolm andAhnesjö 2005). Since oVspring within demersal eggsare unable to leave unfavourable environments (e.g.adverse thermal conditions), parental care behavior ispivotal to enhancing embryonic survival and hatchlingphenotype (reviewed in Mousseau and Fox 1998). Thepresent study emphasises the complexity of combinedparental and environmental eVects that ultimatelyshape the variability and magnitude of larval supply toreef environments.
Acknowledgments We thank Vanessa Messmer and the staV atLizard Island Research Station for assistance with the experi-ment, and Chris Chambers, Martial Depczynski, Charles Fox,Bridget Green and two anonymous reviewers for valuable com-ments on an earlier version of the manuscript. Financial supportwas provided by a Ph.D. fellowship from the AFUW-Qld (M.G.)and research funding from an Australian Research Council Dis-covery grant (M.I.M., M.G.M). This study was conducted underappropriate permits from the Great Barrier Reef Marine ParkAuthority and the JCU Animal Ethics Committee (ApprovalNumber A836_03).
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