How do climate-linked sex ratios and dispersal limit range boundaries?

Annals of Occupational and Environmental Medicine

Maria Boyle²  Lisa E Schwanz¹  Jim Hone²  Arthur Georges² 

[1] School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney NSW 2052, Australia

[2] Institute for Applied Ecology, University of Canberra, Canberra ACT 2601, Australia

关键词: TSD;    Sex ratio;    Reptiles;    Range limits;    Population dynamics;    GSD;    Dispersal;   

Others  :  834351
DOI  :  10.1186/1472-6785-14-19

 received in 2014-04-06, accepted in 2014-06-11,  发布年份 2014

【 摘 要 】

Background

Geographic ranges of ectotherms such as reptiles may be determined strongly by abiotic factors owing to causal links between ambient temperature, juvenile survival and individual sex (male or female). Unfortunately, we know little of how these factors interact with dispersal among populations across a species range. We used a simulation model to examine the effects of dispersal, temperature-dependent juvenile survival and sex determining mechanism (temperature-dependent sex determination (TSD) and genotypic sex determination (GSD)) and their interactions, on range limits in populations extending across a continuous range of air temperatures. In particular, we examined the relative importance of these parameters for population persistence to recommend targets for future empirical research.

Results

Dispersal influenced the range limits of species with TSD to a greater extent than in GSD species. Whereas male dispersal led to expanded species ranges across warm (female-producing) climates, female dispersal led to expanded ranges across cool (male-producing) climates. Two-sex dispersal eliminated the influence of biased sex ratios on ranges.

Conclusion

The results highlight the importance of the demographic parameter of sex ratio in determining population persistence and species range limits.

【 授权许可】

   
2014 Boyle et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Kearney M, Porter W: Mechanistic niche modelling: combining physiological and spatial data to predict species’ ranges. Ecol Lett 2009, 12(4):334-350.
• [2]Sexton JP, McIntyre PJ, Angert AL, Rice KJ: Evolution and ecology of species range limits. Annu Rev Ecol Evol Syst 2009, 40:415-436.
• [3]Mustin K, Benton TG, Dytham C, Travis JMJ: The dynamics of climate-induced range shifting; perspectives from simulation modelling. Oikos 2009, 118(1):131-137.
• [4]Pearson RG, Dawson TP: Predicting the impacts of climate change on the distribution of species: are bioclimate envelope models useful? Glob Ecol Biogeogr 2003, 12(5):361-371.
• [5]Hampe A: Bioclimate envelope models: what they detect and what they hide. Glob Ecol Biogeogr 2004, 13(5):469-471.
• [6]Schloss CA, Nunez TA, Lawler JJ: Dispersal will limit ability of mammals to track climate change in the Western Hemisphere. Proc Natl Acad Sci U S A 2012, 109(22):8606-8611.
• [7]le Roux PC, Virtanen R, Heikkinen RK, Luoto M: Biotic interactions affect the elevational ranges of high-latitude plant species. Ecography 2012, 35(11):1048-1056.
• [8]Kubisch A, Holt RD, Poethke H-J, Fronhofer EA: Where am I and why? Synthesizing range biology and the eco-evolutionary dynamics of dispersal. Oikos 2014, 123(1):5-22.
• [9]Travis JMJ, Delgado M, Bocedi G, Baguette M, Barton K, Bonte D, Boulangeat I, Hodgson JA, Kubisch A, Penteriani V, Saastamoinen M, Stevens VM, Bullock JM: Dispersal and species’ responses to climate change. Oikos 2013, 122(11):1532-1540.
• [10]Krebs CJ: Ecology. The Experimental Analysis of Distribution and Abundance. 6th edition. New York: Benjamin Cummings; 2009.
• [11]Kubisch A, Fronhofer EA: Dispersal, evolution and range dynamics - a synthesis. Oikos 2014, 123(1):3-4.
• [12]Mitchell NJ, Janzen FJ: Temperature-dependent sex determination and contemporary climate change. Sex Dev 2010, 4(1–2):129-140.
• [13]Kallimanis AS: Temperature dependent sex determination and climate change. Oikos 2010, 119(1):197-200.
• [14]Janzen FJ, Paukstis GL: Environmental sex determination in reptiles -ecology, evolution, and experimental-design. Q Rev Biol 1991, 66(2):149-179.
• [15]Hawkes LA, Broderick AC, Godfrey MH, Godley BJ: Investigating the potential impacts of climate change on a marine turtle population. Glob Chang Biol 2007, 13:923-932.
• [16]Escobedo-Galvan AH, Gonzalez-Salazar C, Lopez-Alcaide S, Arroyo-Pena VB, Martinez-Meyer E: Will all species with temperature-dependent sex determination respond the same way to climate change? A reply to Kallimanis (2010). Oikos 2011, 120(5):795-799.
• [17]Hays GC, Broderick AC, Glen F, Godley BJ: Climate change and sea turtles: a 150-year reconstruction of incubation temperatures at a major marine turtle rookery. Glob Chang Biol 2003, 9(4):642-646.
• [18]Hawkes LA, Broderick AC, Godfrey MH, Godley BJ: Climate change and marine turtles. Endanger Species Res 2009, 7(2):137-154.
• [19]Wapstra E, Uller T, Sinn DL, Olsson M, Mazurek K, Joss J, Shine R: Climate effects on offspring sex ratio in a viviparous lizard. J Anim Ecol 2009, 78(1):84-90.
• [20]Schwanz LE, Spencer RJ, Bowden RM, Janzen FJ: Climate and predation dominate juvenile and adult recruitment in a turtle with temperature-dependent sex determination. Ecology 2010, 91(10):3016-3026.
• [21]Telemeco RS, Abbott KC, Janzen FJ: Modeling the effects of climate change induced shifts in reproductive phenology on temperature-dependent traits. Am Nat 2013, 181(5):637-648.
• [22]Witt MJ, Hawkes LA, Godfrey MH, Godley BJ, Broderick AC: Predicting the impacts of climate change on a globally distributed species: the case of the loggerhead turtle. J Exp Biol 2010, 213(6):901-911.
• [23]Georges A, Beggs K, Young JE, Doody JS: Modelling development of reptile embryos under fluctuating temperature regimes. Physiol Biochem Zool 2005, 78(1):18-30.
• [24]Rankin DJ, Kokko H: Do males matter? The role of males in population dynamics. Oikos 2007, 116(2):335-348.
• [25]Broderick AC, Godley BJ, Hays GC: Metabolic heating and the prediction of sex ratios for green turtles (Chelonia mydas). Physiol Biochem Zool 2001, 74(2):161-170.
• [26]Pearse DE, Janzen FJ, Avise JC: Multiple paternity, sperm storage, and reproductive success of female and male painted turtles (Chrysemys picta) in nature. Behav Ecol Sociobiol 2002, 51(2):164-171.
• [27]Hays GC, Fossette S, Katselidis KA, Schofield G, Gravenor MB: Breeding periodicity for male Sea turtles, operational Sex ratios, and implications in the face of climate change. Conserv Biol 2010, 24(6):1636-1643.
• [28]Freedberg S, Taylor DR: Sex ratio variance and the maintenance of environmental sex determination. J Evol Biol 2007, 20(1):213-220.
• [29]Doody JS, Moore JA: Conceptual model for thermal limits on the distribution of reptiles. Herpetol Conserv Biol 2011, 5(2):283-289.
• [30]Olsson M, Shine R: Female-biased natal and breeding dispersal in an alpine lizard, Niveoscincus microlepidotus. Biol J Linn Soc 2003, 79(2):277-283.
• [31]Dubey S, Brown GP, Madsen T, Shine R: Male-biased dispersal in a tropical Australian snake (Stegonotus cucullatus, Colubridae). Mol Ecol 2008, 17(15):3506-3514.
• [32]Doughty P, Sinervo B, Burghardt GM: Sex-biased dispersal in a polygynous lizard, Uta stansburiana. Anim Behav 1994, 47:227-229.
• [33]Rassmann K, Tautz D, Trillmich F, Gliddon C: The microevolution of the Galápagos marine iguana Amblyrhynchus cristatus assessed by nuclear and mitochondrial genetic analyses. Mol Ecol 1997, 6(5):437-452.
• [34]Rivera PC, Gardenal CN, Chiaraviglio M: Sex‒biased dispersal and high levels of gene flow among local populations in the argentine boa constrictor, Boa constrictor occidentalis. Austral Ecol 2006, 31(8):948-955.
• [35]Keogh JS, Webb JK, Shine R: Spatial genetic analysis and long-term mark-recapture data demonstrate male-biased dispersal in a snake. Biol Lett 2007, 3(1):33-35.
• [36]Laurent L, Casale P, Bradai MN, Godley BJ, Gerosa G, Broderick AC, Schroth W, Schierwater B, Levy AM, Freggi D, Abd El-Mawla NEM, Hadoud DA, Gomati HE, Domingo M, Hadjichristophorou M, Kornaraky L, Dmirayak F, Ch G: Molecular resolution of marine turtle stock composition in fishery bycatch: a case study in the Mediterranean. Mol Ecol 1998, 7(11):1529-1542.
• [37]Casale P, Laurent L, Gerosa G, Argano R: Molecular evidence of male-biased dispersal in loggerhead turtle juveniles. J Exp Mar Biol Ecol 2002, 267(2):139-145.
• [38]Roberts MA, Schwartz TS, Karl SA: Global population genetic structure and male-mediated gene flow in the green sea turtle (Chelonia mydas): analysis of microsatellite loci. Genetics 2004, 166(4):1857-1870.
• [39]Bowen B, Karl S: Population genetics and phylogeography of sea turtles. Mol Ecol 2007, 16(23):4886-4907.
• [40]Morreale SJ, Gibbons JW, Congdon JD: Significance of activity and movement in the yellow-bellied slider turtle (Pseudemys scripta). Can J Zool 1984, 62(6):1038-1042.
• [41]Mockford SW, McEachern L, Herman TB, Synder M, Wright JM: Population genetic structure of a disjunct population of Blanding’s turtle (Emydoidea blandingii) in Nova Scotia. Can Biol Conserv 2005, 123(3):373-380.
• [42]Brown GP, Brooks RJ: Sexual and seasonal differences in activity in a northern population of snapping turtles. Chelydra serpentina Herpetologica 1993, 49(3):311-318.
• [43]Garant D, Forde SE, Hendry AP: The multifarious effects of dispersal and gene flow on contemporary adaptation. Funct Ecol 2007, 21(3):434-443.
• [44]Heppell SS: Application of life-history theory and population model analysis to turtle conservation. Copeia 1998, 2:367-375.
• [45]Birchard GF: Effects of Incubation Temperature. In Reptilian Incubation Environment, Evolution and Behaviour. Edited by Deeming DC. Nottingham, UK: Nottingham University Press; 2004:103-123.
• [46]Yntema CL, Mrosovsky N: Critical periods and pivotal temperatures for sexual-differentiation in loggerhead sea turtles. Can J Zool-Revue Canadienne De Zoologie 1982, 60(5):1012-1016.
• [47]Schwarzkopf L, Brooks RJ: Nest-site selection and offspring Sex-ratio in painted turtles, chrysemys-picta. Copeia 1987, 1:53-61.
• [48]Steyermark AC, Spotila JR: Body temperature and maternal identity affect snapping turtle (Chelydra serpentina) righting response. Copeia 2001, 4:1050-1057.
• [49]Chapman DS, Dytham C, Oxford GS: Modelling population redistribution in a leaf beetle: an evaluation of alternative dispersal functions. J Anim Ecol 2007, 76(1):36-44.
• [50]Moilanen A: SPOMSIM: software for stochastic patch occupancy models of metapopulation dynamics. Ecol Model 2004, 179(4):533-550.
• [51]Menard A, Marceau DJ: Exploration of spatial scale sensitivity in geographic cellular automata. Environ Plann B-Plann Des 2005, 32(5):693-714.
• [52]Karl SA, Bowen BW, Avise JC: Global population genetic structure and male-mediated gene flow in the green turtle (Chelonia mydas): RFLP analyses of anonymous nuclear loci. Genetics 1992, 131(1):163-173.
• [53]Ewert MA, Lang JW, Nelson CE: Geographic variation in the pattern of temperature-dependent sex determination in the American snapping turtle (Chelydra serpentina). J Zool 2005, 265:81-95.
• [54]Morjan CL: How rapidly can maternal behavior affecting primary sex ratio evolve in a reptile with environmental sex determination? Am Nat 2003, 162(2):205-219.
• [55]Doody JS, Guarino E, Georges A, Corey B, Murray G, Ewert M: Nest site choice compensates for climate effects on sex ratios in a lizard with environmental sex determination. Evol Ecol 2006, 270:3-15.
• [56]Mazaris AD, Kallimanis AS, Pantis JD, Hays GC: Phenological response of sea turtles to environmental variation across a species’ northern range. Proc R Soc B-Biol Sci 2013, 280:1751.
• [57]Le Galliard JF, Fitze PS, Ferriere R, Clobert J: Sex ratio bias, male aggression, and population collapse in lizards. Proc Natl Acad Sci U S A 2005, 102(50):18231-18236.