Morph-specific and sex-specific temperature effects on morphology in the colour polymorphic damselfly Ischnura elegans

in Animal Biology
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?



Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.



Help

Have Institutional Access?



Access content through your institution. Any other coaching guidance?



Connect

Colour polymorphic species with extensive ranges often exhibit large-scale geographic patterns of morph frequency variation. Because colour polymorphism is associated with correlated differences in multiple traits, such as thermal performance, a likely proximate explanation for such patterns is morph-specific responses to temperature variation. The colour polymorphic Blue-tailed damselfly Ischnura elegans exhibits large-scale geographic variation in morph frequencies, but the possibility that temperature is a proximate explanation for the latitudinal cline in morph frequencies has only ever been tested within a single developmental stage (egg survival and hatching time), where no difference between the morphs was found. I therefore carried out a temperature manipulation on larvae of I. elegans which I raised to maturity in the laboratory. I found that individuals exhibited incomplete compensatory growth after being exposed to cold temperatures, and that individuals which did not emerge successfully and those that experienced cold temperatures had more juvenile morphology in the last instar. In addition, there were sex-specific and morph-specific effects of temperature on adult morphology, such that sexual size dimorphism was increased when individuals experienced warm temperatures throughout the larval stage, and that cold temperatures tended to result in larger size of androchromes and their offspring compared to the other morphs. These results are generally consistent with the large-scale geographic variation in morph frequencies found in this species.

Morph-specific and sex-specific temperature effects on morphology in the colour polymorphic damselfly Ischnura elegans

in Animal Biology

Sections

References

AbbottJ.SvenssonE.I. (2005) Phenotypic and genetic variation in emergence and development time of a trimorphic damselfly. J. Evol. Biol.181464-1470.

AbbottJ.K.BedhommeS.ChippindaleA.K. (2010) Sexual conflict in wing size and shape in Drosophila melanogaster. J. Evol. Biol.231989-1997.

AbbottJ.K.BenschS.GosdenT.P.SvenssonE.I. (2008) Patterns of differentiation in a colour polymorphism and in neutral markers reveal rapid genetic changes in natural damselfly populations. Mol. Ecol.171597-1604.

AbbottJ.K.GosdenT.P. (2009) Correlated morphological and colour differences among females of the damselfly Ischnura elegans. Ecol. Entomol.34378-386.

AbbottJ.K.SvenssonE.I. (2008) Ontogeny of sexual dimorphism and phenotypic integration in heritable morphs. Evol. Ecol.22103-121.

AbbottJ.K.SvenssonE.I. (2010) Morph-specific variation in intersexual genetic correlations in an intraspecific mimicry system. Evol. Ecol. Res.12105-118.

AhnesjöJ.ForsmanA. (2006) Differential habitat selection by pygmy grasshopper color morphs; interactive effects of temperature and predator avoidance. Evol. Ecol.20235-257.

AliM.NiciezaA.WoottonR.J. (2003) Compensatory growth in fishes: a response to growth depression. Fish and Fisheries4147-190.

AngillettaM.J.Jr.SteuryT.D.SearsM.W. (2004) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Int. Comp. Biol.44498-509.

AskewR.R. (1988) The Dragonflies of Europe. Harley BooksColchester, Essex.

BarrettS.C.H.HarderL.D.ColeW.W. (2004) Correlated evolution of floral morphology and mating-type frequencies in a sexually polymorphic plant. Evolution58964-975.

BenkeA.C. (1970) A method for comparing individual growth rates of aquatic insects with special reference to the Odonata. Ecology51328-331.

BolkerB.M.BrooksM.E.ClarkC.J.GeangeS.W.PoulsenJ.R.StevensM.H.H.WhiteJ.-S.S. (2008) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol. Evol.24127-135.

BotsJ.De BruynL.Van DammeR.Van GossumH. (2008) Effects of phenotypic variation onto body temperature and flight activity in a polymorphic insect. Physiological entomology33138-144.

BotsJ.De BruynL.van DongenS.SmoldersR.Van GossumH. (2009) Female polymorphism, condition differences, and variation in male harassment and ambient temperature. Biol. J. Linn. Soc.97545-554.

BoutonN.IserbytA.Van GossumH. (2011) Thermal plasticity in life-history traits in the polymorphic blue-tailed damselfly, Ischnura elegans: no differences between female morphs. Journal of Insect Science11112.

ChangH.-W.EmlenJ.M. (1993) Seasonal variation of microhabitat distribution of the polymorphic land snail Cepaea nemoralis. Oecologia93501-507.

CockA.G. (1966) Genetical aspects of metrical growth and form in animals. Q. Rev. Biol.41131-190.

CookL.M. (1998) A two-stage model for Cepaea polymorphism. Phil. Trans. R. Soc. Lond. B Biol. Sci.3531577-1593.

CooperI.A. (2010) Ecology of sexual dimorphism and clinal variation of coloration in a damselfly. Am. Nat.176566-572.

CorbetP.S. (1999) Dragonflies: Behaviour and Ecology of Odonata. Harley BooksColchester, Essex.

de BlockM.StoksR. (2003) Adaptive sex-specific life history plasticity to temperature and photoperiod in a damselfly. J. Evol. Biol.16986-995.

de BlockM.McPeekM.A.StoksR. (2008) Stronger compensatory growth in a permanent-pond Lestes damselfly relative to temporary-pond Lestes. Oikos117245-254.

de JongP.W.BrakefieldP.M. (1998) Climate and change in clines for melanism in the two-spot labybird, Adalia bipunctata (Coleoptera: Coccinellidae). Proc. R. Soc. Lond. B Biol. Sci.26539-43.

FrazierM.R.HarrisonJ.F.KirktonS.D.RobertsS.P. (2008) Cold-rearing improves cold-flight performance in Drosophila via changes in wing morphology. J. Exp. Biol.2112116-2122.

GaleottiP.RuboliniD.DunnP.O.FasolaM. (2003) Colour polymorphism in birds: causes and functions. J. Evol. Biol.16635-646.

GilchristG.W.HueyR.B. (2004) Plastic and genetic variation in wing loading as a function of temperature within and among parallel clines in Drosophila subobscura. Int. Comp. Biol.44461-470.

GosdenT.P.SvenssonE.I. (2007) Female sexual polymorphism and fecundity consequences of male mating harassment in the wild. PLoS One2e580.

GosdenT.P.SvenssonE.I. (2008) Spatial and temporal dynamics in a sexual selection mosaic. Evolution62845-856.

GosdenT.P.SvenssonE.I. (2009) Density-dependent male mating harassment, female resistance and male mimicry. Am. Nat.173709-721.

GosdenT.P.StoksR.SvenssonE.I. (2011) Range limits, large-scale biogeographic variation, and localized evolutionary dynamics in a polymorphic damselfly. Biol. J. Linn. Soc.102775-785.

GrossM.R. (1991) Evolution of alternative reproductive strategies: frequency-dependent sexual selection in male bluegill sunfish. Phil. Trans. R. Soc. Lond. B Biol. Sci.33259-66.

HammersM.Van GossumH. (2008) Variation in female morph frequencies and mating frequencies: random, frequency-dependent harassment or male mimicry? Anim. Behav.761403-1410.

HarperG.R.Jr.PfennigD.W. (2007) Mimicry on the edge: why do mimics vary in resemblance to their model in different parts of their geographical range? Proc. R. Soc. Lond. B Biol. Sci.2741955-1961.

HedrickP.W. (1986) Genetic polymorphism in heterogeneous environments: a decade later. Annu. Rev. Ecol. Syst.17535-566.

IserbytA.BotsJ.TingJ.J.JvostovF.P.ForbesM.R.SherrattT.N.Van GossumH. (2009) Multi-annual variation in female morph frequencies of the polymorphic damselfly, Nehalennia irene, at continental and regional scales. Animal Biology59313-326.

IserbytA.BotsJ.van DongenS.TingJ.J.Van GossumH.SherrattT.N. (2011) Frequency-dependent variation in mimetic fidelity in an intraspecific mimicry system. Proc. R. Soc. Lond. B Biol. Sci.2783116-3122.

LandM.F. (1997) Visual acuity in insects. Annu. Rev. Entomol.42147-177.

McKinnonJ.S.PierottiM.R. (2010) Colour polymorphism and correlated characters: genetic mechanisms and evolution. Mol. Ecol.195101-5125.

MundayP.L.EyreP.J.JonesG.P. (2003) Ecological mechanisms for coexistence of colour polymorphism in a coral-reef fish: an experimental evaluation. Oecologia137519-526.

OxfordG.S. (2005) Genetic drift within a protected polymorphism: enigmatic variation in color-morph frequencies in the candy-stripe spider, Enoplognatha ovata. Evolution592170-2184.

PartridgeL.BarrieB.FowlerK.FrenchV. (1994) Evolution and development of body size and cell size in Drosophila melanogaster in response to temperature. Evolution481269-1276.

Phifer-RixeyM.HeckmanM.TrussellG.C.SchmidtS. (2008) Maintenance of clinal variation for shell colour phenotype in the flat periwinkle Littorina obtusata. J. Evol. Biol.21966-978.

PotvinC. (2001) ANOVA, experimental layout and analysis. In: ScheinerS.M.GurevitchJ. (Eds.) Design and Analysis of Ecological Experiments2nd[4]63-76. Oxford University PressOxford, UK.

PowellA.M.DavisM.PowellJ.R. (2010) Phenotypic plasticity across 50 MY of evolution: Drosophila wing size and temperature. Journal of Insect Physiology56380-382.

RiceW.R.ChippindaleA.K. (2001) Intersexual ontogenetic conflict. J. Evol. Biol.14685-693.

RutowskiR.L.WarrantE.J. (2002) Visual field structure in the Empress Leilia Asterocampa leilia (Lepidoptera, Nymphalidae): dimentions and regional variation in acuity. J. Comp. Physiol. A1881-12.

Sánchez-GuillénR.A.Van GossumH.Cordero RiveraA. (2005) Hybridization and the inheritance of female colour polymorphism in two Ischnurid damselflies (Odonata: Coenagrionidae). Biol. J. Linn. Soc.85471-481.

Sánchez-GuillénR.A.HanssonB.WellenreutherM.SvenssonE.I.Cordero RiveraA. (2011) The influence of stochastic and selective forces in the population divergence of female colour polymorphism in damselflies of the genus Ischnura. Heredity107513-522.

SAS Institute Inc. (2007) JMP. [7.0.2].

SchemskeD.W.BierzychudekP. (2007) Spatial differentiation for flower color in the desert annual Linanthus parryae: was Wright right? Evolution612528-2543.

SinervoB.LivelyC.M. (1996) The rock-paper-scissors game and the evolution of alternative male strategies. Nature380240-243.

StoksR.de BlockM. (2011) Rapid growth reduces cold resistance: evidence from latitudinal variation in growth rate, cold resistance and stress proteins. PLoS One6e16935.

SvenssonE.I.AbbottJ. (2005) Evolutionary dynamics and population biology of a polymorphic insect. J. Evol. Biol.181503-1514.

SvenssonE.I.AbbottJ.HärdlingR. (2005) Female polymorphism, frequency-dependence and rapid evolutionary dynamics in natural populations. Am. Nat.165567-576.

SvenssonE.I.AbbottJ.K.GosdenT.P.CoreauA. (2008) Female polymorphisms, sexual conflict and limits to speciation processes in animals. Evol. Ecol.2393-108.

TakahashiY.YoshimuraJ.MoritaS.WatanabeM. (2010) Negative frequency-dependent selection in female color polymorphism of a damselfly. Evolution643620-3628.

TakahashiY.MoritaS.YoshimuraJ.WatanabeM. (2011) A geographic cline induced by negative frequency-dependent selection. BMC Evol. Biol.11256.

TeraiY.SeehausenO.SasakiA.TakahashiK.MizoiriS.SugawaraT.SatoT.WatanabeM.KonijnendijkN.MrossoH.D.J.TachidaH.ImaiH.ShichidaY.OkadaN. (2006) Divergent selection on opsins drives incipient speciation in Lake Victoria cichlids. PLoS Biol.4e433.

Van GossumH.BeirinckxK.ForbesM.R.SherrattT.N. (2007) Do current hypotheses explain continental and seasonal variation in female morph frequencies of the damselfly, Nehalennia irene? Biol. J. Linn. Soc.90501-508.

WellenreutherM.Sánchez-GuillénR.A.Cordero RiveraA.SvenssonE.I.HanssonB. (2011) Environmental and climatic determinants of molecular diversity and genetic population structure in a Coenarionid damselfly. PLoS One6e20440.

ZiembaK.S.RutowskiR.L. (2000) Sexual dimorphism in eye morphology in a butterfly (Asterocampa leilia; Lepidoptera, Nymphalidae). Psyche10325-36.

Figures

  • View in gallery

    Differences in size over development for (a) maternal morph, (b) sex, (c) emergence success, and (d) temperature. Centroid size was calculated from 11 landmarks (see fig. 2a) and time in the figure indicates two-week intervals relative to the date of emergence (or death, for individuals that died in the last instar). Offspring of infuscans-obsoleta females were initially smaller than offspring of the other morphs, but this difference decreased over ontogeny. Females were larger than males throughout ontogeny, but this difference was only significant in the final instars. Individuals that emerged successfully were significantly larger than individuals that did not emerge successfully in the last instar. Individuals that had experienced cold temperatures during part of development were smaller than those that had been in warm conditions, and although individuals in the cold treatment increased their rate of growth once they were returned to warm conditions they did not fully compensate for the difference in size. There were no significant interactions between main effects, so only main effects are shown. Bonferroni-corrected significance indicators: t=P<0.10, =P<0.05, =P<0.01, =P<0.001. Symbols show LS means and SEs.

  • View in gallery

    Landmarks used in the analysis of larval shape (a) and differences in the last instar (b-e). (a) 11 landmarks were placed along the outline and midline of the larva. (b) Differences between the offspring of the three female morphs in the last instar. The grid shows how the mean infuscans or infuscans-obsoleta offspring shape must be deformed to produce the mean configuration found in androchrome offspring (note that both deformation grids are exaggerated by a factor of 5 for clarity). Offspring of androchrome females have significantly different morphology than offspring of infuscans or infuscans-obsoleta females, with smaller heads, larger eyes, and relatively longer abdomens (compare with (c)). (c) Differences between the sexes in the last instar. The grid shows how the female configuration must be deformed to produce a male configuration (exaggerated by a factor of 10 for clarity). Males have larger eyes, a narrower thorax, and a longer, thinner abdomen than females. (d) Differences in the last instar between larvae that emerged successfully and those that did not. The grid shows deformation of the successful configuration to the unsuccessful configuration (exaggerated by a factor of 3 for clarity). Individuals that did not emerge successfully had a more juvenile configuration than those that did. (e) Differences in the last instar between individuals that experienced warm conditions or cold conditions during development. The grid shows deformation of the warm configuration to the cold configuration (exaggerated by a factor of 5 for clarity). Individuals that experienced cold conditions had a more juvenile configuration than those that experience warm conditions throughout. This figure is published in colour in the online version.

  • View in gallery

    Effect of maternal morph on offspring sex ratio. Offspring of infuscans females had the lowest probability of successful emergence. Infuscans-obsoleta females produced the most female-biased broods. There were no significant interactions between main effects, so only main effects are shown. Symbols show means and SEs.

Information

Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 57 57 26
Full Text Views 38 38 25
PDF Downloads 10 10 2
EPUB Downloads 2 2 0