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Evolutionary allometry of sexual dimorphism of jumping performance in anurans

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Abstract

Sexual dimorphism is a common feature in animals, yet the degree of sexual dimorphism is not constant across taxa. Sometimes the magnitude of sexual dimorphism varies systematically with body size, resulting in evolutionary allometry of sexual dimorphism. While such patterns are commonly investigated for traits such as overall size, allometric variation in sexual dimorphism of other traits remains underexplored. Here, we characterize the evolutionary allometry of sexual dimorphism in a functional phenotypic trait (jumping performance) in anurans. Using morphology and anatomical approximations of jumping performance across 146 species, we test for evidence of the correlated selection model of sexual dimorphism evolution. We analyze patterns of evolutionary allometry of sexual dimorphism in key phenotypic traits, including: body size (snout-vent length and mass), relative leg length, relative leg muscle volume, mass-specific peak jumping energy, and peak jumping velocity. We find that as previously reported, sexual size dimorphism scales isometrically between species and is independent of sexual dimorphism in jumping performance. Notably, however, we found significant trends in the evolutionary allometry of sexual dimorphism in relative limb length, and in two components of jumping performance. Additionally, we found greater rates of evolution for females versus males in relative limb length, but not jumping performance. We also observed that the allometric trends in limb length dimorphism were related to performance allometry. Sexual dimorphism in jumping performance increased in species with high performance while females in high performance species displayed increased relative limb length. Thus, we hypothesize that selection acting on functional performance explains allometric patterns of sexual dimorphism in morphology. We discuss biological implications of our findings in relation to natural and sexual selection. This study highlights the types of insights one may gain by studying the allometry of sexual dimorphism from a functional perspective to learn about both patterns and processes in evolution.

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All data may be found in Dryad.

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All code associated with this manuscript may be found at https://github.com/bhjuarez/allometry-dimorphism-jumping.

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References

  • Abouheif E, Fairbairn DJ (1997) A comparative analysis of allometry for sexual size dimorphism: Assessing Rensch’s rule. Am Nat 149:540–562

    Article  Google Scholar 

  • Adams DC (2013) Comparing evolutionary rates for different phenotypic traits on a phylogeny using likelihood. Syst Biol 62:181–192

  • Adams DC (2014) A generalized K statistic for estimating phylogenetic signal from shape and other high-dimensional multivariate data. Syst Biol 63:685–697

    Article  PubMed  Google Scholar 

  • Adams DC, Glynne E, Kaliontzopoulou A (2020) Interspecific allometry for sexual shape dimorphism: Macroevolution of multivariate sexual phenotypes with application to Rensch’s rule. Evolution 74:1908–1922

    Article  PubMed  Google Scholar 

  • Adams DC, Collyer ML, Kaliontzopoulou A et al (2021) Geomorph: Software for geometric morphometric analyses. R package version 4.0.0.99. https://cran.r-project.org/package=geomorph

  • AmphibiaWeb (2021) < https://amphibiaweb.org> University of California, Berkeley, CA, USA. Accessed 11 Jul 2021

  • Anderson RA, Vitt LJ (1990) Sexual selection versus alternative causes of sexual dimorphism in teiid lizards. Oecologia 84:145–157

    Article  PubMed  Google Scholar 

  • Arnold SJ (1983) Morphology, performance and fitness. Am Zool 23:347–361

    Article  Google Scholar 

  • Astley HC (2016) The diversity and evolution of locomotor muscle properties in anurans. J Exp Biol 219:3163–3173

    Article  PubMed  Google Scholar 

  • Astúa D (2010) Cranial sexual dimorphism in New World marsupials and a test of Rensch’s rule in Didelphidae. J Mammal 91:1011–1024

    Article  Google Scholar 

  • Baeza JA, Asorey CM (2012) Testing the role of male–male competition in the evolution of sexual dimorphism: A comparison between two species of porcelain crabs. Biol J Linn Soc Lond 105:548–558

    Article  Google Scholar 

  • Bastos RP, Haddad CFB (1997) Predation on the toad Bufo crucifer during reproduction (Anura: Bufonidae). Amphib-reptil 18:295–298

    Article  Google Scholar 

  • Bell RC, Zamudio KR (2012) Sexual dichromatism in frogs: Natural selection, sexual selection and unexpected diversity. Proc Biol Sci 279:4687–4693

    PubMed  PubMed Central  Google Scholar 

  • Berry JF, Shine R (1980) Sexual size dimorphism and sexual selection in turtles (order testudines). Oecologia 44:185–191

    Article  PubMed  Google Scholar 

  • Blanckenhorn WU (2005) Behavioral causes and consequences of sexual size dimorphism. Ethology 111:977–1016

    Article  Google Scholar 

  • Blanckenhorn WU, Stillwell RC, Young KA et al (2006) When Rensch meets Bergmann: Does sexual size dimorphism change systematically with latitude? Evolution 60:2004–2011

  • Bonduriansky R (2007) Sexual selection and allometry: A critical reappraisal of the evidence and ideas. Evolution 61:838–849

    Article  PubMed  Google Scholar 

  • Burbrink FT, Futterman I (2019) Female-biased gape and body-size dimorphism in the New World watersnakes (tribe: Thamnophiini) oppose predictions from Rensch’s rule. Ecol Evol 9:9624–9633

    Article  PubMed  PubMed Central  Google Scholar 

  • Cabrera MP, Scrocchi GJ, Cruz FB (2013) Sexual size dimorphism and allometry in Liolaemus of the L. laurenti group (Sauria: Liolaemidae): Morphologic lability in a clade of lizards with different reproductive modes. Zool Anz 252:299–306

    Article  Google Scholar 

  • Ceballos CP, Adams DC, Iverson JB et al (2013) Phylogenetic patterns of sexual size dimorphism in turtles and their implications for Rensch’s rule. Evol Biol 40:194–208

    Article  Google Scholar 

  • Cheng C, Houle D (2020) Predicting multivariate responses of sexual size dimorphism to direct and indirect selection. Am Nat 196:391–405

    Article  PubMed  Google Scholar 

  • Colwell RK (2000) Rensch’s rule crosses the line: Convergent allometry of sexual size dimorphism in hummingbirds and flower mites. Am Nat 156:495–510

    Article  PubMed  Google Scholar 

  • Cox RM, Butler MA, John-Alder HB (2007) The evolution of sexual size dimorphism in reptiles. In: Fairbairn DJ, Blanckenhorn WU, Székely T (eds) Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism. Oxford University Press, New York, pp 38–49

    Chapter  Google Scholar 

  • Dale J, Dunn PO, Figuerola J et al (2007) Sexual selection explains Rensch’s rule of allometry for sexual size dimorphism. Proc Biol Sci 274:2971–2979

    PubMed  PubMed Central  Google Scholar 

  • De Lisle SP, Rowe L (2013) Correlated evolution of allometry and sexual dimorphism across higher taxa. Am Nat 182:630–639

    Article  PubMed  Google Scholar 

  • Denton JSS, Adams DC (2015) A new phylogenetic test for comparing multiple high-dimensional evolutionary rates suggests interplay of evolutionary rates and modularity in lanternfishes (Myctophiformes; Myctophidae). Evolution 69:2425–2440

    Article  PubMed  Google Scholar 

  • Emlen DJ, Hunt J, Simmons LW (2005) Evolution of sexual dimorphism and male dimorphism in the expression of beetle horns: Phylogenetic evidence for modularity, evolutionary lability, and constraint. Am Nat 166(Suppl 4):S42–S68

    Article  PubMed  Google Scholar 

  • Endler JA (1984) Natural and sexual selection on color patterns in poeciliid fishes. In: Zaret TM (ed) Evolutionary ecology of neotropical freshwater fishes, 1st edn. Springer, Dordrecht, pp 95–111

    Chapter  Google Scholar 

  • Fairbairn DJ (1997) Allometry for sexual size dimorphism: Pattern and process in the coevolution of body size in males and females. Annu Rev Ecol Syst 28:659–687

    Article  Google Scholar 

  • Fairbairn DJ, Preziosi RF (1996) Sexual selection and the evolution of sexual size dimorphism in the water strider, Aquarius remigis. Evolution 50:1549–1559

    Article  PubMed  Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Feng YJ, Blackburn DC, Liang D et al (2017) Phylogenomics reveals rapid, simultaneous diversification of three major clades of Gondwanan frogs at the Cretaceous-Paleogene boundary. Proc Natl Acad Sci USA 114:E5864–E5870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grant V (1963) The origin of adaptations. Columbia University Press, New York

    Google Scholar 

  • Han X, Fu J (2013) Does life history shape sexual size dimorphism in anurans? A comparative analysis. BMC Evol Biol 13:1–11

    Article  Google Scholar 

  • Hansen TF, Bartoszek K (2012) Interpreting the evolutionary regression: the interplay between observational and biological errors in phylogenetic comparative studies. Syst Biol 61:413–425

    Article  PubMed  Google Scholar 

  • Harmon LJ, Weir JT, Brock CD et al (2008) GEIGER: Investigating evolutionary radiations. Bioinformatics 24:129–131

    Article  CAS  PubMed  Google Scholar 

  • Hirst AG, Kiørboe T (2014) Macroevolutionary patterns of sexual size dimorphism in copepods. Proc Biol Sci 281:20140739

    PubMed  PubMed Central  Google Scholar 

  • Hunt J, Breuker CJ, Sadowski JA et al (2009) Male-male competition, female mate choice and their interaction: Determining total sexual selection. J Evol Biol 22:13–26

    Article  PubMed  Google Scholar 

  • Ives AR, Midford PE, Garland T Jr (2007) Within-species variation and measurement error in phylogenetic comparative methods. Syst Biol 56:252–270

    Article  PubMed  Google Scholar 

  • Johnson PJ, Noonan MJ, Kitchener AC et al (2017) Rensching cats and dogs: Feeding ecology and fecundity trends explain variation in the allometry of sexual size dimorphism. R Soc Open Sci 4:170453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Juarez BH, Moen DS, Adams DC (2020) A morphological method to approximate jumping performance in anurans for macroevolutionary studies. Evol Biol 47:260–271

    Article  Google Scholar 

  • Kaliontzopoulou A, Carretero MA, Llorente GA (2007) Multivariate and geometric morphometrics in the analysis of sexual dimorphism variation in Podarcis lizards. J Morphol 268:152–165

    Article  PubMed  Google Scholar 

  • Kaliontzopoulou A, Carretero MA, Adams DC (2015) Ecomorphological variation in male and female wall lizards and the macroevolution of sexual dimorphism in relation to habitat use. J Evol Biol 28:1–15

    Article  Google Scholar 

  • Kilmer JT, Rodríguez RL (2017) Ordinary least squares regression is indicated for studies of allometry. J Evol Biol 30:4–12

    Article  CAS  PubMed  Google Scholar 

  • Kuo C-Y, Gillis GB, Irschick DJ (2011) Loading effects on jump performance in green anole lizards, Anolis carolinensis. J Exp Biol 214:2073–2079

    Article  PubMed  Google Scholar 

  • Land R (1980) Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34:292–305

    Article  Google Scholar 

  • Liao WB, Zeng Y, Zhou CQ et al (2013) Sexual size dimorphism in anurans fails to obey Rensch’s rule. Front Zool 10:1–7

    Google Scholar 

  • Logan ML, Neel LK, Nicholson DJ et al (2021) Sex-specific microhabitat use is associated with sex-biased thermal physiology in Anolis lizards. J Exp Biol 224:jeb235697

    PubMed  Google Scholar 

  • Lovich JE, Gibbons JW (1992) A review of techniques for quantifying sexual size dimorphism. Growth Dev Aging 56:269–281

    CAS  PubMed  Google Scholar 

  • Martins EP, Hansen TF (1997) Phylogenies and the comparative method: A general approach to incorporating phylogenetic Information into the analysis of interspecific data. Am Nat 149:646–667

    Article  Google Scholar 

  • Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge

    Book  Google Scholar 

  • Moen DS (2019) What determines the distinct morphology of species with a particular ecology? The roles of many-to-one mapping and trade-offs in the evolution of frog ecomorphology and performance. Am Nat 194:E81–E95

    Article  PubMed  Google Scholar 

  • Monnet JM, Cherry MI (2002) Sexual size dimorphism in anurans. Proc Biol Sci 269:2301–2307

    Article  PubMed  PubMed Central  Google Scholar 

  • Nali RC, Zamudio KR, Haddad CFB et al (2014) Size-dependent selective mechanisms on males and females and the evolution of sexual size dimorphism in frogs. Am Nat 184:727–740

    Article  PubMed  Google Scholar 

  • Owens IPF, Hartley IR (1998) Sexual dimorphism in birds: Why are there so many different forms of dimorphism? Proc Royal Soc B 265:397–407

    Article  Google Scholar 

  • Peñalver-Alcázar M, Galán P, Aragón P (2019) Assessing Rensch’s rule in a newt: Roles of primary productivity and conspecific density in interpopulation variation of sexual size dimorphism. J Biogeogr 46:2558–2569

    Article  Google Scholar 

  • Peplowski MM, Marsh RL (1997) Work and power output in the hindlimb muscles of Cuban tree frogs Osteopilus septentrionalis during jumping. J Exp Biol 200:2861–2870

    Article  CAS  PubMed  Google Scholar 

  • Pincheira-Donoso D, Hunt J (2017) Fecundity selection theory: Concepts and evidence. Biol Rev Camb Philos Soc 92:341–356

    Article  PubMed  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, et al (2021) nlme: Linear and nonlinear mixed effects models. R package version 3.1–152, URL: https://CRAN.R-project.org/package=nlme

  • Price T, Birch GL (1996) Repeated evolution of sexual color dimorphism in passerine birds. Auk 113:842–848

    Article  Google Scholar 

  • Portik DM, Blackburn DC, McGuire JA (2020) Macroevolutionary patterns of sexual size dimorphism among African tree frogs (Family: Hyperoliidae). J Hered 111:379–391

    Article  PubMed  Google Scholar 

  • Prestwich KN (1994) The energetics of acoustic signaling in anurans and insects. Integr Comp Biol 34:625–643

    Google Scholar 

  • R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/

  • Rand AS (1985) Tradeoffs in the evolution of frog calls. Proc Anim Sci 94:623–637

    Article  Google Scholar 

  • Reeve JP, Fairbairn DJ (2001) Predicting the evolution of sexual size dimorphism. J Evol Biol 14:244–254

    Article  Google Scholar 

  • Reilly SM, Jorgensen ME (2010) The evolution of jumping in frogs: Morphological evidence for the basal anuran locomotor condition and the radiation of locomotor systems in crown group anurans. J Morph 272:149–168

    Article  PubMed  Google Scholar 

  • Reiss MJ (1986) Sexual dimorphism in body size: Are larger species more dimorphic? J Theor Biol 121:163–172

    Article  Google Scholar 

  • Rensch B (1960) Evolution above the species level. Columbia University Press, New York

    Google Scholar 

  • Revell LJ (2012) phytools: An R packagefor phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223

    Article  Google Scholar 

  • Ryan MJ, Tuttle MD, Rand AS (1982) Bat predation and sexual advertisement in a neotropical anuran. Am Nat 119:136–139

    Article  Google Scholar 

  • Selander RK (1966) Sexual dimorphism and differential niche utilization in birds. Condor 68:113–151

    Article  Google Scholar 

  • Serrano-Meneses MA, Córdoba-Aguilar A, Azpilicueta-Amorín M et al (2008) Sexual selection, sexual size dimorphism and Rensch’s rule in Odonata. J Evol Biol 21:1259–1273

    Article  CAS  PubMed  Google Scholar 

  • Shine R (1979) Sexual selection and sexual dimorphism in the Amphibia. Copeia 1979:297–306

    Article  Google Scholar 

  • Silva NR, Berneck BVM, da Silva HR et al (2020) Egg-laying site, fecundity and degree of sexual size dimorphism in frogs. Biol J Linn Soc Lond 131:600–610

    Article  Google Scholar 

  • Stuart-Fox DM, Ord TJ (2004) Sexual selection, natural selection and the evolution of dimorphic coloration and ornamentation in agamid lizards. Proc Royal Soc B 271:2249–2255

    Article  Google Scholar 

  • Taigen TL, Wells KD (1985) Energetics of vocalization by an anuran amphibian (Hyla versicolor). J Comp Physiol B 155:163–170

    Article  Google Scholar 

  • Wainwright PC, Alfaro ME, Bolnick DI et al (2005) Many-ton-one mapping of form to function: A general principle of organismal design? Integr Comp Biol 45:256–262

    Article  PubMed  Google Scholar 

  • Wcislo WT (1989) Behavioral environments and evolutionary change. Annu Rev Ecol Syst 20:137–169

    Article  Google Scholar 

  • West-Eberhard MJ (1986) Alternative adaptations, speciation, and phylogeny (a review). Proc Natl Acad Sci USA 83:1388–1392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst 20:249–278

    Article  Google Scholar 

  • Wharton DI, Wright IJ, Falster DS et al (2006) Bivariate line-fitting methods for allometry. Biol 81:259–291

    Google Scholar 

  • Zeng Z-B (1988) Long-term correlated response, interpopulation covariation, and interspecific allometry. Evolution 42:363–374

    Article  PubMed  Google Scholar 

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Acknowledgements

This work was supported by a National Science Foundation Graduate Research Fellowship (to BHJ), National Science Foundation Grant DBI-1902511 (to DCA), and a California Academy of Natural Sciences Michele L. Aldrich Collections Research Grant (to BHJ). We thank Andres Vargas for help with data collection, Elizabeth Glynne for helpful discussions, Anne Bronikowski, Philip Dixon, and two reviewers for useful insight. Finally, we are indebted to the many museum curators and collection managers that made this work possible.

Funding

This work was supported by a National Science Foundation Graduate Research Fellowship (to BHJ), National Science Foundation Grant DBI-1902511 (to DCA), and a California Academy of Natural Sciences Michele L. Aldrich Collections Research Grant (to BHJ).

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All authors contributed to the study conception and design. Material preparation, data collection, and analyses were performed by Bryan H. Juarez. The first draft of the manuscript was written by Bryan H. Juarez and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Bryan H. Juarez.

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Juarez, B.H., Adams, D.C. Evolutionary allometry of sexual dimorphism of jumping performance in anurans. Evol Ecol 36, 717–733 (2022). https://doi.org/10.1007/s10682-021-10132-x

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