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Development timeandsize-related traits in the oriental blowfly

Development time and size-related traits in the oriental blow?y,Chrysomya megacephala along a latitudinal gradient from China

Yuwei Hu 1,Xi Yuan 1,Fen Zhu n ,Chaoliang Lei

Hubei Insect Resources Utilization and Sustainable Pest Management Key laboratory,College of Plant Science and Technology,Huazhong Agricultural University,Wuhan 430070,Hubei,China

a r t i c l e i n f o

Article history:

Received 17March 2010Accepted 30July 2010Keywords:

Development time Body size Temperature

Population-by-temperature

a b s t r a c t

Organisms can respond to variation in temperature through the direct effect of temperature on phenotypes (phenotypic plasticity),or through long-term adaptation to temperature (and thus evolution of either mean size or thermal reaction norm).We examined the effects of various temperatures (of 20and 301C)on development time,adult body size (body length and body width)and pre-adult survivorship in six populations of Chrysomya megacephala ,collected at different latitudes.We found that temperature changes induced substantial plasticity in terms of development time,body size and pre-adult survivorship,indicating that developmental temperature signi?cantly affects growth and life history traits of C.megacephala .We also detected genetic differences among populations for body size and development time,and these two traits exhibited highly signi?cant variations in the responses of different populations to various temperature conditions,indicating genetic differences among populations in terms of thermal reaction norms.The latitude of origin of the different populations (and hence mean temperature regimes in the environments from where the populations originated)did not appear to fully explain these genetic differences.In short,changes in development time and body size in C.megacephala can be regarded as adaptations to changing thermal regimes.

1.Introduction

Growth and life history traits of many ectothermic animals are strongly affected by temperature.For example,development time and body size generally decrease with increase in temperature (temperature–size rule;Carleton,1960;Vannote and Sweeny,1980;Lonsdale and Levinton,1985;Atkinson,1994;Partridge et al.,1994;Van der Have and de Jong,1996;Atkinson and Sibly,1997;Ramsden and Elek,1998;Chown and Gaston,1999;Reeve et al.,2000;Kingsolver and Huey,2008).However,a contrary rule —the hotter is better —proposes that genotypes or species with relatively high optimal temperatures also have relatively high maximal performance or ?tness (Kingsolver and Huey,2008).These phenotypic responses may be a result of a temperature effect on the organism’s physiology during development (devel-opmental plasticity)or may be a consequence of adaptation to different thermal environments (Stillwell and Fox,2005).Adaptive (genetic)and developmental (nongenetic)hypotheses are often debated when examining the extent to which organisms are in?uenced by temperature-mediated natural selection or by the

environmental effects of temperature and how this differentially affects the phenotypic traits of a particular organism (Van Voorhies,1996,1997;Mousseau,1997;Partridge and Coyne,1997;Angilletta and Dunham,2003;Stillwell and Fox,2005).Studies of patterns of geographic variation often give evidences for genetic adaptation to temperature (Stillwell and Fox,2009).For instance,organisms often show clines in body size (Blanckenhorn and Demont,2004)that persist after rearing in a common environment (Partridge and Coyne,1997).In Drosophila melanogaster ,body size clines are often repeatable across continent (James et al.,1995;Van’t Land et al.,1999)and evolve fast following colonization of new continents (Huey et al.,2000).Plastic responses of body size and other traits to developmental temperature are also widespread,and frequently parallel geo-graphic in traits (Stillwell et al.,2010).For example,adult body size of some ectothermic animals decreased or increased with increase in developmental temperature (Atkinson,1994;Kingsolver and Huey,2008).Because nongenetic responses to developmental temperature are thus nearly identical to those produced by evolution at different temperatures,it can be dif?cult to distinguish genetic adaptation vs.phenotypic plasticity in natural https://www.wendangku.net/doc/074420614.html,mon garden experiments are required to disentangle these factors (e.g.Stillwell and Fox,2005).Further-more,adaptation to different thermal environments could gene-rate populations varying in the degree or direction of plasticity

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journal homepage:https://www.wendangku.net/doc/074420614.html,/locate/jtherbio

Journal of Thermal Biology

Corresponding author.Tel./fax:+862787287207.E-mail address:ioir@https://www.wendangku.net/doc/074420614.html, (F.Zhu).1

Both authors contributed equally to this work.

Journal of Thermal Biology 35(2010)366–371

they exhibited in response to temperature,which result in variation among populations in thermal reaction norms (Morin et al.,1999;Gilchrist and Huey,2004;Stillwell and Fox,2005;Kingsolver et al.,2007;Stillwell et al.,2010).

Adult body size and development time are key traits that are not only consequences of temperature-dependent processes but also causes of variation in ?tness (Kingsolver and Huey,2008).Although adult body size is not a ?tness component itself,increased size often confers advantages in terms of fecundity and survival in adults at non-stressful temperatures (Partridge and Fowler,1993;Norry et al.,2001;Sambucetti et al.,2006).Fast development (i.e.a decrease age to maturity)will increase ?tness in some species of Diptera such as Drosophila either by increasing larval survival under wild conditions or probability of early reproduction,in cases where all other factors are constant (Roff,2000;Norry et al.,2001;Sambucetti et al.,2006)though fast growth (i.e.a fast grow rate)can be energetically costly and increases the risk of starvation and predation in some insects (e.g.Gotthard,2000;Gotthard et al.,1994;Stillwell et al.,2010).

We compare thermal reaction norms for six populations of the blow?ies,Chrysomya megacephala ,from China using a common garden experiment at two temperatures.These six populations occurred at different latitudes and were subject to different local thermal environments.We expect that these populations are adapted to ‘‘warm’’and ‘‘cool’’environments and should be genetically differentiated in a number of traits.First,we quantify the relative contribution of genetically based differentiation vs.plasticity in generating variation in body size.Second,we test whether norms of reaction vary among populations.

2.Materials and methods 2.1.Study populations

C.megacephala (Diptera)are oriental blow?ies (Zhao et al.,2009a,b )and exposed to a considerable variation in climatic condition from tropical climate to subtropical climate.They are mainly scavengers,feeding on dead organic matter such as dead animals.We used six C.megacephala populations collected from different geographic localities in China.These populations spanned 22.3–30.521N in latitude and 16.6–221C in mean annual temperature (Table 1).We performed a common garden experiment at two temperatures (20and 301C)to examine temperature-induced plasticity,genetic differences among populations and genetic (population level)variation in temperature-induced plasticity for development time,body length,body width and pre-adult survivorship.These temperatures we used are within the range of temperatures normally encountered in the ?eld (daily temperature range from 17to 391C during late summer and early fall when blow?ies are most active;/https://www.wendangku.net/doc/074420614.html,/S ;China Meteorological Data Sharing Service System).

2.2.Details

All test populations were passed through two generations of identical rearing conditions to obtain more offspring and to eliminate nongenetic parental thermal environment effects before the experimental assays described below were performed.All individuals per population were reared in a standard cage (50?40?30cm)that was made with a glass roof and gauze on ?ve of the sides.Adults were supplied daily with granular sucrose,water and ?sh ?esh (?sh hereafter).Water was supplied by dipping a piece of sponge as a wick in a bottle ?lled with water,and the ?sh was provided in a Petri dish.The ?rst-instar larvae were randomly collected from the cage and transferred to a fresh piece of ?sh with 70%RH wheat bran placed in a rearing bottle

Table 1

Populations of Chrysomya megacephala collected from various locations in China.Annual mean temperature,January temperature (minimal temperature)and July temperature (maximal temperature)were obtained from weather stations located nearest to each collection locality (China Meteorological Data Sharing Service System /https://www.wendangku.net/doc/074420614.html,/S )for a recent 30-year period.Population Longitude (1W)/latitude (1N)January temperature (1C)July temperature (1C)Annual mean temperature (1C)Guangdong 113.52/22.313.628.622Fujian 117.35/24.5212.527.820.4Hunan 113/28.21 4.928.617.1Jiangxi 115.89/28.68 5.329.217.6Zhejiang 120.19/30.26 4.328.416.5Hubei

114.31/30.52

3.7

28.7

16.6

Table 2

Analysis of variance (type III sums of squares)for the effects of population,sex and rearing temperature on pre-adult survivorship,development times and body size (body length and body width)of Chrysomya megacephala.Effect

Body length Population 531.29o 0.001Temperature 1243.56o 0.001Sex

153.01o 0.001Population ?temperature 5 2.490.036Population ?sex 5 2.690.025Sex ?temperature

1 4.620.034Population ?sex ?temperature 50.150.979

Error 96Total

120Body width Population 521.68o 0.001Temperature 1115.87o 0.001Sex

116.70o 0.001Population ?temperature 5 2.940.016Population ?sex 5 3.340.008Sex ?temperature

1 5.490.021Population ?sex ?temperature 50.690.634

Error 96Total

120Development time Population 574.95o 0.001Temperature 110764.33

o 0.001Sex

1 2.630.108Population ?temperature 553.92o 0.001Population ?sex 50.0440.999Sex ?temperature 10.0890.766

Total

120Pre-adult survivorship Population 5 2.330.057Temperature

110.350.002Population ?temperature 5 1.330.268

Error 48Total

Y.Hu et al./Journal of Thermal Biology 35(2010)366–371367

(height ?10cm,diameter ?7cm)covered with muslin secured with a rubber band.There were 40individuals per bottle,which was big enough to eliminate potential larval competition.Sixty rearing bottles in total were immediately placed at two con-stant-temperature regimes (of 20and 301C),with 5bottles per population per temperature (i.e.5bottles ?2rearing temperatures ?6populations ?60bottles in total).The emerged adults from the bottles were transferred to adult cages described above and were smoked with ethyl ether until they were not ?ying.Then,body length (from vertex of the head to the end of the abdomen)and body width (the greatest width across body)for each adult were immediately measured using a vernier caliper calibrated to the nearest 0.1mm.In total,2400offspring were raised to adult evenly divided among the two rearing temperatures.Devel-opmental time at each temperature was checked simultaneously for all six populations every 12h until adult eclosion.Pre-adult survivorship was obtained as the percentage of adult blow?ies emerging per bottle,considering each bottle as data point

and pooling both sexes (as sex was not recognized in the ?rst stadium).

2.3.Statistical analysis

Statistical analyses were done with SPSS 13.0using ANOVA (type III sums of squares)to determine the effects of sex,population,temperature and interactions (i.e.sex ?temperature;population ?temperature;sex ?population;sex ?temperature-?population)on body size (body length and body width;e.g.Norry et al.,2001;Stillwell and Fox,2005,2009).Each bottle was considered as a data point.

3.Results

Body size of both males and females increased with increase in temperature (F 1,120?243.56,P o 0.0001for body

length;

Fig.1.Adult body length (from vertex of the head to the end of the abdomen)and body width (the greatest width across body)of females (A,C)and males (B,D)of populations of Chrysomya megacephala raised at two different temperatures (20and 301C).Standard errors (71SE)are included.

Y.Hu et al./Journal of Thermal Biology 35(2010)366–371

368

F 1,120?115.87,P o 0.0001for body width;Table 2;Fig.1)inconsistent with the general pattern in ectothermic animals (Atkinson,1994).Blow?ies took shorter time to develop at higher temperature (F 1,120?10,764.33,P o 0.001;Fig.2;Table 2).Pre-adult survivorship was higher at high (301C)temperature than at low (201C)temperature (F 1,60?10.35,P ?0.002;Table 2;Fig.3).

There were differences among the six populations in body size (F 5,120?31.29,P o 0.0001for body length;F 5,120?21.68,P o 0.0001for body width;Table 2;Fig.1)and development time (F 5,120?74.95,P o 0.0001;Fig.2).Signi?cant differences were

detected between populations in development time at 201C (F 5,29?36.57,P o 0.0001for female;F 5,29?93.28,P o 0.0001for male;Fig.2),but a complete homogeneity was seen among populations at 301C (F 5,29?2.14,P ?0.095for female;F 5,29?0.993,P ?0.443for male;Fig.2).The response to tempera-ture differed considerably among populations for body length (F 5,120?2.49,P ?0.036;Table 2;Fig.1),body width (F 5,120?2.94,P ?0.016;Table 2;Fig.1)and development time (F 5,96?53.92,P o 0.001;Fig.2),indicating genetic differentiation among populations in thermal reaction norms.There were weak differences among the six populations for pre-adult survivorship (Table 2;F 5,60?2.33,P ?0.057),and this trait showed no population-by-temperature interaction (Table 2;F 5,60?1.33,P ?0.268).

4.Discussion

Temperature profoundly affects growth and life history traits in ectothermic animals through selection (i.e.,genetic)and through direct effects on the phenotype (i.e.,nongenetic/plasticity;Stillwell et al.,2010).In this study we collected six populations of C.megacephala from different latitudes (Table 1).Substantial temperature-induced plasticity for certain traits (development time,body length,body width and pre-adult survivorship)was observed in C.megacephala .Body size (body length and body width)and pre-adult survivorship increased with increase in temperature,but develop-ment time decreased with increase in temperature.In addition,we detected genetic differences among populations and variation among populations in thermal reaction norms for body size and development time.The shape of the thermal reaction norms did not conform to predictions based on adaptation to temperature —we predicted lower latitude populations to mature larger at high temperature (compared with higher latitude populations)and higher latitude populations to mature larger at low temperature,but this was not observed.

When organisms experience spatial and temporal variation in temperature,population differentiation in thermal reaction norms is expected to evolve (Stillwell et al.,2010).Recent studies have shown population differentiation in thermal reaction

norms

https://www.wendangku.net/doc/074420614.html,rval development times of females (A)and males (B)of populations of Chrysomya megacephala raised at two different temperatures (20and 301C).Standard errors (71SE)are

included.

Fig.3.Pre-adult survivorship of populations of Chrysomyia megacephala raised at two different temperatures (20and 301C).Standard errors (71SE)are included.

Y.Hu et al./Journal of Thermal Biology 35(2010)366–371369

for body size(Morin et al.,1999;Gilchrist and Huey,2004; Stillwell and Fox,2005;Kingsolver et al.,2007),survivorship and development time(Norry et al.,2001;Bochdanovits and de Jong, 2003).Take Pieris rapae,a cabbage white butter?y;for example, body size decreases with increase in temperature in a population from Washington,USA,whereas body size increases with increase in rearing temperature in a population from North Carolina,USA (Kingsolver et al.,2007).The Washington population experiences strong selection for size under cooler conditions,whereas the North Carolina population experiences strong selection for body size under warm conditions,which generates different slopes in these reaction norms.We found population differentiation in thermal reaction norms(i.e.population-by-temperature interac-tions)for body size and other traits in this current study. However,the populations did not respond in the predicted directions based on their origin of latitude(i.e.the highest latitude populations were not the largest at low temperature while simultaneously the smallest at high temperature).One possible explanation is that temperature is not the major climatic variable driving the evolution of clines in these blow?ies(e.g. Stillwell et al.,2007;Stillwell and Fox,2009),although it may partially contribute to clines in body size.Recent studies(e.g. Stillwell et al.,2007;Stillwell and Fox,2009)suggest that some environmental variables,such as moisture,host plant and seasonality,along the latitudinal cline affect selection on body size.Our study cannot test whether temperature variation along the cline generates the selection that produced the observed pattern in body size.It is more likely that other variables contribute to selection producing geographic variation in body size.Furthermore,Van der Have and de Jong(1996)suggested that differential thermal sensitivity of enzymes that control cellular growth and differentiation could cause popula-tion?temperature interactions.The populations experience different thermal environments,so enzymes that control growth and differentiation possibly have evolved different thermal sensitivities,resulting in the variation in body size and develop-ment time that we found among populations.However,the mechanisms underlying these phenomena need further study. Another possible explanation is that the temperatures we used in our study are non-?uctuating,though the temperatures we chose were based on the temperatures blow?ies are likely to experience in the?eld during the time when blow?ies are most likely to be active in China(Methods).If we use?uctuating temperatures that include periods of lower or higher stress,our results might better re?ect experiences that occur in nature(Kingsolver et al.,2007).

Overall,population?temperature interaction is a necessary condition for adaptation of a particular trait to temperature (Norry et al.,2001)and the present results show that thermal adaptation is evident for development time and body size in C. megacephala.

Acknowledgements

We thank Yongjian Xie,Rangyu Mo,Yong Wang and Xiaomin Chen for assistance with?eld collections.We also thank two anonymous referees for their helpful comments and suggestions on the manuscript.This research was supported by National Facilities and Information Infrastructure for Science and Technology Program(2005DKA21105).

References

Atkinson, D.,1994.Temperature and organism size—a biological law for ectotherms?Adv.Ecol.Res.25,1–58.Atkinson, D.,Sibly,R.M.,1997.Why are organisms usually bigger in colder environments?Making sense of a life history puzzle.Trends Ecol.Evol.12, 235–239.

Angilletta,M.J.,Dunham,A.E.,2003.The temperature–size rule in ectotherms: simple evolutionary explanations may not be general.Am.Nat.162,333–342. Blanckenhorn,W.U.,Demont,M.,2004.Bergmann and converse Bergmann latitudinal clines in arthropods:two ends of a continuum?https://www.wendangku.net/doc/074420614.html,p.Biol.

44,413–424.

Bochdanovits,Z.,de Jong,G.,2003.Temperature dependence of?tness compo-nents in geographical populations of Drosophila melanogaster:changing the association between size and?tness.Biol.J.Linn.Soc.80,717–725. Carleton,R.,1960.The application of Bergmann’s and Allen’s rules to the poikilotherms.J.Morphol.106,85–108.

Chown,S.L.,Gaston,K.J.,1999.Exploring links between physiology and ecology at macro-scales:the role of respiratory metabolism in insects.Biol.Rev.74, 87–120.

Gilchrist,G.W.,Huey,R.B.,2004.Plastic and genetic variation in wing loading as a function of temperature within and among parallel clines in Drosophila https://www.wendangku.net/doc/074420614.html,p.Biol.44,461–470.

Gotthard,K.,2000.Increased risk of predation as a cost of high growth rate:an experimental test in a butter?y.J.Anim.Ecol.69,896–902.

Gotthard,K.,Nylin,S.,Wiklund,C.,1994.Adaptive variation in growth rate:life history costs and consequences in the speckled wood butter?y,Pararge aegeria.

Oecologia99,281–289.

Huey,R.B.,Gilchrist,G.W.,Carlson,M.L.,Berrigan,D.,Serra,L.,2000.Rapid evolution of a geographic cline in size in an introduced?y.Science287,308–309. James,A.C.,Azevedo,R.B.R.,Partridge,L.,1995.Cellular basis and developmental timing in a size cline of Drosophila melanogaster in laboratory and?eld populations.Genetics140,659–666.

Kingsolver,J.G.,Huey,R.B.,2008.Size,temperature,and?tness:three rules.Evol.

Ecol.Res.10,251–268.

Kingsolver,J.G.,Massie,K.R.,Smith,M.H.,2007.Rapid population divergence in thermal reaction norms for an invading species:breaking the temperature–size rule.J.Evol.Biol.20,892–900.

Lonsdale, D.J.,Levinton,J.S.,https://www.wendangku.net/doc/074420614.html,titudinal differentiation in copepod growth—an adaptation to temperature.Ecology66,1397–1497.

Morin,J.P.,Moreteau,B.,Pe′tavy,G.,David,J.R.,1999.Divergence of reaction norms of size characters between tropical and temperate populations of Drosophila melanogaster and D.simulans.J.Evol.Biol.12,329–339.

Mousseau,T.A.,1997.Ectotherms follow the converse to Bergmann’s rule.

Evolution51,630–632.

Norry,F.M.,Bubliy,O.A.,Loeschcke,V.,2001.Development time,body size and wing loading in Drosophila buzzatii from lowland and highland populations in Argentina.Hereditas135,35–40.

Partridge,L.,Fowler,K.,1993.Direct and correlated responses to selection on thorax length in Drosophila melanogaster.Evolution47,213–226.

Partridge,L.,Barrie,B.,Fowler,K.,French,V.,1994.Evolution and development of body size and cell size in Drosophila melanogaster in response to temperature.

Evolution48,1269–1276.

Partridge,L.,Coyne,J.A.,1997.Bergmann’s rule in ectotherms:is it adaptive?

Evolution51,632–635.

Ramsden,N.,Elek,J.A.,1998.Life cycle and development rates of the leaf beetle Chrysophtharta agricola(Chapuis)(Coleoptera:Chrysomelidae)on Eucalyptus nitens at two temperature regimens.Aus.J.Entomol.37,238–242.

Reeve,M.W.,Fowler,K.,Partridge,L.,2000.Increased body size confers greater ?tness at lower experimental temperature in male Drosophila melanogaster.J.

Evol.Biol.13,836–844.

Roff, D.A.,2000.Tradeoff between growth and reproduction:an analysis of quantitative genetic evidence.J.Evol.Biol.13,434–445.

Sambucetti,P.,Loeschcke,V.,Norry, F.M.,2006.Development time and size-related traits in Drosophila buzzatii along an altitudinal gradient from Argentina.Hereditas143,77–83.

Stillwell,R.C.,Fox,C.W.,https://www.wendangku.net/doc/074420614.html,plex patterns of phenotypic plasticity:interactive effects of temperature during rearing and oviposition.Ecology86,924–934. Stillwell,R.C.,Morse,G.E.,Fox,C.W.,2007.Geographic variation in body size and sexual size dimorphism of a seed-feeding beetle.Am.Nat.170,358–369. Stillwell,R.C.,Fox, C.W.,2009.Geographic variation in body size,sexual size dimorphism and?tness components of a seed-feeding beetle:local adaptation versus phenotypic plasticity.Oikos118,703–712.

Stillwell,R.C.,Blanckenhorn,W.U.,Teder,T.,Fox,C.W.,2010.Sex differences in phenotypic plasticity affect variation in sexual size dimorphism in insects: from physiology to evolution.Ann.Rev.Entomol.55,227–245.

Van der Have,T.M.,de Jong,G.,1996.Adult size in ectotherms:temperature effects on growth and differentiation.J.Theor.Biol.183,329–340.

Van Voorhies,W.A.,1996.Bergmann size clines:a simple explanation for their occurrence in ectotherms.Evolution50,1259–1264.

Van Voorhies,W.A.,1997.On the adaptive nature of Bergmann size clines:a reply to Mousseau,Partridge and Coyne.Evolution51,635–640.

Vannote,R.L.,Sweeny,B.W.,1980.Geographic analysis of thermal equilibria:a conceptual model for evaluating the effect of natural and modi?ed thermal regimes on aquatic insect communities.Am.Nat.115,667–695.

Van’t Land,J.P.,van Putten,P.,Zwaan,B.,et al.,https://www.wendangku.net/doc/074420614.html,titudinal variation in wild populations of Drosophila melanogaster:heritabilities and reactions norm.J.

Evol.Biol.12,222–232.

Y.Hu et al./Journal of Thermal Biology35(2010)366–371 370

Zhao,F.,Chen,B.,Wang,Y.,Zhu,F.,Lei,C.L.,2009a.Eicosanoids mediate nodulation reactions to bacterial Escherichia coli K12infections in larvae of the oriental blow?y,Chrysomya megacephala.Insect Sci.16,387–392.Zhao, F.,Stanley, D.,Wang,Y.,Zhu, F.,Lei, C.L.,2009b.Eicosanoids mediate nodulation reactions to a mollicute bacterium in larvae of the blow?y, Chrysomya megacephala.J.Insect Physiol.55,192–196.

Y.Hu et al./Journal of Thermal Biology35(2010)366–371371