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Fecundity Selection and the Evolution of Reproductive Output and Sex-Specific Body Size in the Liolaemus Lizard Adaptive Radiation

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Abstract

Fecundity is a primary component of fitness. Theory predicts that the evolution of fecundity through increased brood size results from fecundity selection favouring larger female size to accommodate more offspring and to store more energy. This is expected to generate asymmetric selection on body size between the sexes, ultimately driving evolution of female-biased sexual size dimorphism. Additionally, it has been predicted that the intensity of fecundity selection increases when the opportunities for reproduction are reduced by the limiting thermal effects of increasing latitude-elevation (i.e. decreasing environmental temperatures) on the length of the reproductive season. This later factor would be particularly strong among ectotherms, where reproduction is heavily temperature-dependent. However, this integrative perspective on reproductive evolution by fecundity selection has rarely been investigated. Here, we employ a comparative approach to investigate these predictions in Liolaemus, a prominent lizard radiation. As expected, Liolaemus reproductive output (i.e. offspring number per reproductive episode) increases predictably with increasing female size. However, contrary to predictions, we found that increased fecundity does not translate into female-biased SSD, and that combined latitude-elevation does not impose a detectable effect on fecundity. Finally, our allometric analyses reveal that SSD scales with body size, which supports the occurrence of Rensch’s rule in these lizards. We discuss the evolutionary implications of our results, and the assumptions of the investigated hypotheses.

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References

  • Abdala, C. S. (2007). Phylogeny of the boulengeri group (Iguania: Liolaemidae, Liolaemus) based on morphological and molecular characters. Zootaxa, 1538, 1–84.

    Google Scholar 

  • Abouheif, E., & Fairbairn, D. J. (1997). A comparative analysis of allometry for sexual size dimorphism: Assessing Rensch’s rule. American Naturalist, 149, 540–562.

    Article  Google Scholar 

  • Andersson, M. (1994). Sexual selection. Princeton: Princeton University Press.

    Google Scholar 

  • Ashton, K. G. (2002). Do amphibians follow Bergmann’s rule? Canadian Journal of Zoology, 80, 708–716.

    Article  Google Scholar 

  • Ashton, K. G., & Feldman, C. R. (2003). Bergmann’s rule in nonavian reptiles: turtles follow it, lizards and snakes reverse it. Evolution, 57, 1151–1163.

    PubMed  Google Scholar 

  • Blackburn, D. G. (2000). Reptilian viviparity: past research, future directions, and appropriate models. Comparative Biochemistry and Physiology A, 127, 391–409.

    CAS  Google Scholar 

  • Blanckenhorn, W. U., Dixon, A. F. G., Fairbairn, D. J., Foellmer, M. W., Gibert, P., van der Linde, K., et al. (2007a). Proximate causes of Rensch’s rule: does sexual size dimorphism in arthropods result from sex differences in development time? American Naturalist, 169, 245–257.

    Article  PubMed  Google Scholar 

  • Blanckenhorn, W. U., Meier, R., & Teder, T. (2007b). Rensch’s rule in insects: patterns among and within species. In D. J. Fairbairn, W. U. Blanckenhorn, & T. Szekely (Eds.), Sex, size & gender roles. Evolutionary studies of sexual size dimorphism (pp. 60–70). Oxford: Oxford University Press.

    Google Scholar 

  • Braña, F. (1996). Sexual dimorphism in lacertid lizards: male head increase vs. female abdomen increase. Oikos, 75, 511–523.

    Article  Google Scholar 

  • Brown, R. P., Znari, M., El Mouden, E. L. H., & Harris, P. (1999). Estimating asymptotic body size and testing geographic variation in Agama impalearis. Ecography, 22, 277–283.

    Article  Google Scholar 

  • Calder, W. A. (1984). Size, function and life history. Massachusetts: Harvard University Press.

    Google Scholar 

  • Cei, J. M. (1993). Reptiles del noroeste, nordeste y este de la Argentina. Herpetofauna de las selvas subtropicales, puna y pampas. Museo Regionale di Scienze Naturali di Torino, Torino.

  • Charlesworth, B., & Charlesworth, D. (2010). Elements of evolutionary genetics. Colorado: Roberts and Company.

    Google Scholar 

  • Cox, R. M., Skelly, S. L., & John-Alder, H. B. (2003). A comparative test of adaptive hypotheses for sexual size dimorphism in lizards. Evolution, 57, 1653–1669.

    PubMed  Google Scholar 

  • Cox, R. M., Butler, M., & John-Alder, H. B. (2007). The evolution of sexual size dimorphism in reptiles. In D. J. Fairbairn, W. U. Blanckenhorn, & T. Szekely (Eds.), Sex, size & gender roles. Evolutionary studies of sexual size dimorphism (pp. 38–49). Oxford: Oxford University Press.

    Google Scholar 

  • Cruz, F. B., Fitzgerald, L. A., Espinoza, R. E., & Schulte, J. A. (2005). The importance of phylogenetic scale in tests of Bergmann’s and Rapoport’s rules: lessons from a clade of South American lizards. Journal of Evolutionary Biology, 18, 1559–1574.

    Article  PubMed  CAS  Google Scholar 

  • Darwin, C. (1874). The descent of man and selection in relation to sex (2nd ed.). New York: Appleton.

    Google Scholar 

  • de Queiroz, A., & Ashton, K. G. (2004). The phylogeny of a species-level tendency: species heritability and possible deep origins of Bergmann’s rule in tetrapods. Evolution, 58, 1674–1684.

    Article  PubMed  Google Scholar 

  • Espinoza, R. E., & Lobo, F. (1996). Possible communal nesting in two species of Liolaemus lizards (Iguania: Tropiduridae) from northern Argentina. Herpetological Natural History, 4, 65–68.

    Google Scholar 

  • Espinoza, R. E., Wiens, J. J., & Tracy, C. R. (2004). Recurrent evolution of herbivory in small, cold-climate lizards: breaking the ecophysiological rules of reptilian herbivory. Proceedings of the National Academy of Sciences, USA, 101, 16819–16824.

    Article  CAS  Google Scholar 

  • Fairbairn, D. J. (1997). Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Annual Review of Ecology, Evolution, and Systematics, 28, 659–687.

    Article  Google Scholar 

  • Fairbairn, D. J. (2006). Defining and measuring fitness. In C. W. Fox & J. B. Wolf (Eds.), Evolutionary genetics. Concepts and case studies (pp. 52–54). Oxford: Oxford University Press.

    Google Scholar 

  • Fairbairn, D. J. (2007). The enigma of sexual size dimorphism. In D. J. Fairbairn, W. U. Blanckenhorn, & T. Szekely (Eds.), Sex, size & gender roles. Evolutionary studies of sexual size dimorphism (pp. 1–10). Oxford: Oxford University Press.

    Google Scholar 

  • Fairbairn, D. J., & Shine, R. (1993). Patterns of sexual size dimorphism in seabirds of the southern hemisphere. Oikos, 68, 139–145.

    Article  Google Scholar 

  • Fairbairn, D. J., Blanckenhorn, W. U., & Szekely, T. (2007). Sex, size & gender roles. Evolutionary studies of sexual size dimorphism. Oxford: Oxford University Press.

    Google Scholar 

  • Felsenstein, J. (1985). Phylogenies and the comparative method. American Naturalist, 125, 1–15.

    Article  Google Scholar 

  • Fitch, H. S. (1970). Reproductive cycles in lizards and snakes (Vol. 52, pp. 1–247). University of Kansas Museum of Natural History, Miscellaneous Publications.

  • Fitch, H. S. (1978). Sexual size differences in the genus Sceloporus (Vol. 51, pp. 441–461). University of Kansas Museum of Natural History, Miscellaneous Publications.

  • Fitch, H. S. (1981). Sexual size differences in reptiles (Vol. 70, pp. 1–72). University of Kansas Museum of Natural History, Miscellaneous Publications.

  • Fitch, H. S. 1985. Variation in clutch and litter size in New World reptiles. (Vol. 76, pp. 1–76). University of Kansas Museum of Natural History, Miscellaneous Publications.

  • Freckleton, R. P. (2009). The seven deadly sins of comparative analysis. Journal of Evolutionary Biology, 22, 1367–1375.

    Article  PubMed  CAS  Google Scholar 

  • Frýdlová, P., & Frynta, D. (2010). A test of Rensch’s rule in varanid lizards. Biological Journal of the Linnean Society, 100, 293–306.

    Article  Google Scholar 

  • Garcia-Berthou, E. (2001). On the misuse of residuals in ecology: testing regression residuals vs. the analysis of covariance. Journal of Animal Ecology, 70, 708–711.

    Article  Google Scholar 

  • Garland, T., Harvey, P. H., & Ives, A. R. (1992). Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology, 41, 18–32.

    Google Scholar 

  • Garland, T., Dickerman, A. W., Janis, C. M., & Jones, J. A. (1993). Phylogenetic analysis of covariance by computer simulation. Systematic Biology, 42, 265–292.

    Google Scholar 

  • Ghiselin, M. T. (1974). The economy of nature and the evolution of sex. Berkeley: University of California Press.

    Google Scholar 

  • Green, A. J. (2001). Mass/length residuals: measures of body condition or generators of spurious results? Ecology, 82, 1473–1483.

    Article  Google Scholar 

  • Harvey, P. H., & Pagel, M. D. (1991). The comparative method in evolutionary biology. Oxford: Oxford University Press.

    Google Scholar 

  • Harvey, P. H., & Rambaut, A. (2000). Comparative analyses for adaptive radiations. Philosophical Transactions of the Royal Society of London, B, 355, 1599–1605.

    Article  CAS  Google Scholar 

  • Head, G. (1995). Selection on fecundity and variation in the degree of sexual size dimorphism among spider species (class Araneae). Evolution, 49, 776–781.

    Article  Google Scholar 

  • Husak, J. F., Lappin, A. K., & Van Den Bussche, R. A. (2009). The fitness advantage of a high-performance weapon. Biological Journal of the Linnean Society, 96, 840–845.

    Article  Google Scholar 

  • LaBarbera, M. (1989). Analyzing body size as a factor in ecology and evolution. Annual Review of Ecology and Systematics, 20, 97–117.

    Article  Google Scholar 

  • Losos, J. B. (2009). Lizards in an evolutionary tree. Ecology and adaptive radiation of anoles. California: University of California Press.

    Google Scholar 

  • Losos, J. B., Butler, M., & Schoener, T. W. (2003). Sexual dimorphism in body size and shape in relation to habitat use among species of Caribbean Anolis lizards. In S. F. Fox, J. K. McCoy, & T. A. Baird (Eds.), Lizard social behaviour (pp. 356–380). Baltimore and London: John Hopkins University Press.

    Google Scholar 

  • Lutgens, F. K., & Tarbuck, E. J. (1998). The atmosphere. An introduction to meteorology. New Jersey: Prentice Hall.

    Google Scholar 

  • Martins, E. P. (2004). COMPARE, version 4.6b. Computer programs for the statistical analysis of comparative data. Distributed by the author at http://compare.bio.indiana.edu/. Department of Biology, Indiana University, Indiana.

  • Martins, E. P., & Garland, T. (1991). Phylogenetic analyses of the correlated evolution of continuous characters: a simulation study. Evolution, 45, 534–557.

    Article  Google Scholar 

  • Meiri, S. (2008). Evolution and ecology of lizard body sizes. Global Ecology and Biogeography, 17, 724–734.

    Article  Google Scholar 

  • Peters, R. H. (1983). The ecological implications of body size. Cambridge: Cambridge University Press.

    Google Scholar 

  • Pianka, E. R., & Vitt, L. J. (2003). Lizards. Windows to the evolution of diversity. Berkeley, Los Angeles, London: University of California Press.

    Google Scholar 

  • Pincheira-Donoso, D. (2010). The balance between predictions and evidence and the search for universal macroecological patterns: taking Bergmann’s rule back to its endothermic origin. Theory in Biosciences, 129, 247–253.

    Article  PubMed  Google Scholar 

  • Pincheira-Donoso, D., Scolaro, J. A., & Schulte, J. A. (2007a). The limits of polymorphism in Liolaemus rothi: molecular and phenotypic evidence for a new species of the Liolaemus boulengeri clade (Iguanidae, Liolaemini) from boreal Patagonia of Chile. Zootaxa, 1452, 25–42.

    Google Scholar 

  • Pincheira-Donoso, D., Tregenza, T., & Hodgson, D. J. (2007b). Body size evolution in South American Liolaemus lizards of the boulengeri clade: a contrasting reassessment. Journal of Evolutionary Biology, 20, 2067–2071.

    Article  PubMed  CAS  Google Scholar 

  • Pincheira-Donoso, D., Hodgson, D. J., & Tregenza, T. (2008a). The evolution of body size under environmental gradients in ectotherms: why should Bergmann’s rule apply to lizards? BMC Evolutionary Biology, 8, 68.

    Article  PubMed  Google Scholar 

  • Pincheira-Donoso, D., Scolaro, J. A., & Sura, P. (2008b). A monographic catalogue on the systematics and phylogeny of the South American iguanian lizard family Liolaemidae (Squamata, Iguania). Zootaxa, 1800, 1–85.

    Google Scholar 

  • Pincheira-Donoso, D., Hodgson, D. J., Stipala, J., & Tregenza, T. (2009). A phylogenetic analysis of sex-specific evolution of ecological morphology in Liolaemus lizards. Ecological Research, 24, 1223–1231.

    Article  Google Scholar 

  • Pough, F. H. (1973). Lizard energetics and diet. Ecology, 54, 837–844.

    Article  Google Scholar 

  • Pough, F. H., Andrews, R. M., Cadle, J. E., Crump, M. L., Savitzky, A. H., & Wells, K. D. (2004). Herpetology (3rd ed.). New Jersey: Pearson, Prentice Hall.

    Google Scholar 

  • Powell, G. L. & Russell, A. P. (2007). Life history implications for conservation and monitoring of lizards in Canada. In: C. N. L. Seburn & C. A. Bishop (eds.), Ecology, conservation, and status of reptiles in Canada (pp. 23–40). Herpetological Conservation 2.

  • Reznick, D. N. (1985). Costs of reproduction: an evaluation of the empirical evidence. Oikos, 44, 257–267.

    Article  Google Scholar 

  • Roff, D. A. (2002). Life history evolution. Sunderland: Sinauer Associates.

    Google Scholar 

  • Schluter, D. (2000). The ecology of adaptive radiation. Oxford: Oxford University Press.

    Google Scholar 

  • Schulte, J. A., Macey, J. R., Espinoza, R. E., & Larson, A. (2000). Phylogenetic relationships in the iguanid lizard genus Liolaemus: multiple origins of viviparous reproduction and evidence for recurring Andean vicariance and dispersal. Biological Journal of the Linnean Society, 69, 75–102.

    Article  Google Scholar 

  • Seigel, R. A., & Ford, N. B. (1987). Reproductive ecology. In R. A. Seigel, J. T. Collins, & S. S. Novak (Eds.), Snakes. Ecology and evolutionary biology (pp. 210–252). New York: Macmillan.

    Google Scholar 

  • Shine, R. (1988). The evolution of large body size in females: a critique of Darwin’s “fecundity advantage” model. American Naturalist, 131, 124–131.

    Article  Google Scholar 

  • Shine, R. (1994). Sexual size dimorphism in snakes revisited. Copeia, 1994, 326–346.

    Article  Google Scholar 

  • Shine, R. (2005). Life-history evolution in reptiles. Annual Reviews of Ecology, Evolution and Systematics, 36, 23–46.

    Article  Google Scholar 

  • Sinervo, B. (2000). Adaptation, natural selection, and optimal life-history allocation in the face of genetically based trade-offs. In T. A. Mousseau, B. Sinervo, & J. A. Endler (Eds.), Adaptive genetic variation in the wild (pp. 41–64). Oxford: Oxford University Press.

    Google Scholar 

  • Smith, R. J. (1999). Statistics of sexual size dimorphism. Journal of Human Evolution, 36, 423–459.

    Article  PubMed  CAS  Google Scholar 

  • Sokal, R. R., & Rohlf, F. J. (1995). Biometry: the principles and practice of statistics in biological research. California: W. H. Freeman.

    Google Scholar 

  • Stearns, S. C. (1992). The evolution of life histories. Oxford: Oxford University Press.

    Google Scholar 

  • Stephens, P. R., & Wiens, J. J. (2009). Evolution of sexual size dimorphisms in emydid turtles: ecological dimorphism, Rensch’s rule, and sympatric divergence. Evolution, 63, 910–925.

    Article  PubMed  Google Scholar 

  • Stuart-Fox, D. (2009). A test of Rensch’s rule in dwarf chameleons (Bradypodion spp.), a group with female-biased sexual size dimorphism. Evolutionary Ecology, 23, 425–433.

    Article  Google Scholar 

  • Tabachnick, B. G., & Fidell, L. S. (2007). Using multivariate statistics. Massachusetts: Pearson International.

    Google Scholar 

  • Thornhill, T., & Alcock, J. (1983). The evolution of insect mating systems. Massachusetts: Harvard University Press.

    Google Scholar 

  • Tinkle, D. W., Wilbur, H. M., & Tilley, S. G. (1970). Evolutionary strategies in lizard reproduction. Evolution, 24, 55–74.

    Article  Google Scholar 

  • Trivers, R. (1972). Parental investment and sexual selection. In B. Campbell (Ed.), Sexual selection and the descent of man, 1871–1971 (pp. 136–179). Chicago: Aldine.

    Google Scholar 

  • Vanhooydonck, B., Cruz, F. B., Abdala, C. S., Moreno-Azocar, D. L., Bonino, M. F., & Herrel, A. (2010). Sex-specific evolution of bite performance in Liolaemus lizards (Iguania: Liolaemidae): the battle of the sexes. Biological Journal of the Linnean Society, 101, 461–475.

    Article  Google Scholar 

  • Vitt, L. J. (1986). Reproductive tactics of sympatric gekkonid lizards with a comment on the evolutionary and ecological consequences of invariant clutch size. Copeia, 1986, 773–786.

    Article  Google Scholar 

  • Weiblen, G. D., Oyama, R. K., & Donoghue, M. J. (2000). Phylogenetic analysis of dioecy in monocotyledons. American Naturalist, 155, 46–58.

    Article  PubMed  Google Scholar 

  • Williams, G. C. (1966). Adaptation and natural selection. New Jersey: Princeton University Press.

    Google Scholar 

  • Zamudio, K. R. (1998). The evolution of female-biased sexual size dimorphism: a population-level comparative study in horned lizards (Phrynosoma). Evolution, 52, 1821–1833.

    Article  Google Scholar 

  • Zar, J. H. (2009). Biostatistical analysis. New Jersey: Pearson International.

    Google Scholar 

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Acknowledgments

We are grateful to Wolf Blanckenhorn for advice on a set of quantitative analyses and for providing his excel file prepared for major-axis regressions. Dave Hodgson also provided valuable quantitative advice. This manuscript benefited from discussions and insightful observations made by Jan Stipala. Two anonymous referees provided sharp and insightful observations that made an important contribution to improve this paper. This study was funded by the Leverhulme Trust.

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Correspondence to Daniel Pincheira-Donoso.

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Pincheira-Donoso, D., Tregenza, T. Fecundity Selection and the Evolution of Reproductive Output and Sex-Specific Body Size in the Liolaemus Lizard Adaptive Radiation. Evol Biol 38, 197–207 (2011). https://doi.org/10.1007/s11692-011-9118-7

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