vol. 188, supplement the american naturalist september 2016 Symposium Polyandry, Predation, and the Evolution of Frog Reproductive Modes* Kelly R. Zamudio,1,† Rayna C. Bell,2 Renato C. Nali,3,4 Célio F. B. Haddad,3 and Cynthia P. A. Prado4,‡ 1. Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York 14853; 2. Museum of Vertebrate Zoology, Department of Integrative Biology, University of California, Berkeley, California 94720; and Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560; 3. Departamento de Zoologia, Instituto de Biociências, Universidade Estadual Paulista, Rio Claro, São Paulo, Brazil; 4. Departamento de Morfologia e Fisiologia Animal, Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista, Jaboticabal, São Paulo, Brazil Online enhancements: appendix. Dryad data: http://dx.doi.org/10.5061/dryad.v67g3. fi abstract: Frog reproductive modes are complex phenotypes that diversi ed as egg and clutch characteristics, oviposition site, include egg/clutch characteristics, oviposition site, larval develop- larval development, stage and size of hatchling, and some- ment, and sometimes, parental care. Two evident patterns in the evo- times, parental care (Salthe and Duellman 1973). This com- lution of these traits are the higher diversity of reproductive modes in plexity—and the diversity that arises from variation in the the tropics and the apparent progression from aquatic to terrestrial re- many interconnected components of reproductive modes— production, often attributed to higher fitness resulting from decreased has attracted the attention of biologists for decades (Jameson predation on terrestrial eggs and tadpoles. Here, we propose that sex- 1957; Crump 1974; Duellman 1985). In the past 10 years, we ual selection—and not only natural selection due to predation—fa- fi vors terrestrial breeding by reducing the loss of fitness due to polyan- have made signi cant progress in describing, categorizing, dry. To examine this novel selective mechanism, we reconstructed the and reconstructing the evolution of various traits that are in- evolution of reproductive diversity in two frog families (Hylidae and cluded in reproductive modes (Haddad and Prado 2005; Leptodactylidae) and tested for concerted evolution of egg and tad- Summers et al. 2006; Wells 2007; Crump 2015; Pereira et al. pole development sites with specific mating behaviors. We found that 2015). Two patterns identified in the earliest studies of anuran oviposition and tadpole development sites are evolving independently, reproductive mode are that the diversity in these phenotypes do not show the same diversity and/or directionality in terms of terres- is higher in the tropics (Goin and Goin 1962; Duellman 1985) triality, and thus may be diversifying due to different selective mecha- nisms. In both families, terrestrial egg deposition is correlated with am- and that, especially in those tropical lineages, reproductive plexus that is hidden from competing males, and in hylids, testes mass modes range from the fully aquatic (and, presumably, ances- was significantly larger and more variable in males with exposed am- tral) to increasingly terrestrial reproduction (Lutz 1947; Goin plexus that are vulnerable to polyandry. Our results indicate that in- and Goin 1962; Heyer 1969). Aided by the synthesis of new trasexual selection has been an underappreciated mechanism promot- natural history data and more robust estimates of phyloge- ing diversification of frog reproductive modes. netic relationships, we are now in a position to address not Keywords: Anura, phylogenetic comparative methods, reproduction, only questions about the patterns of distribution of reproduc- sexual selection, multimale spawning. tive modes among species but also about the selective mech- anisms underlying their diversification (Summers and Earn 1999; Monroe and Alonzo 2014). Introduction Previous studies show unequivocally that more terrestrial Anuran reproductive modes are complex modular pheno- reproductive modes in frogs are most common in warmer types that transcend life-history stages and include traits as and wetter environments of the tropics (Goin and Goin 1962; Duellman 1985). Recent analyses of reproductive modes across global anuran communities confirmed that species with ter- * This issue originated as the 2015 Vice Presidential Symposium presented at restrial egg laying or direct development occur in regions the annual meetings of the American Society of Naturalists. with significantly higher precipitation than those with † Corresponding author; e-mail: [email protected]. ‡ ORCIDs: Zamudio, http://orcid.org/0000-0001-5107-6206. aquatic eggs and larvae (Gomez-Mestre et al. 2012), and this Am. Nat. 2016. Vol. 188, pp. S41–S61. q 2016 by The University of Chicago. effect may be mediated by the fact that sites with high precip- 0003-0147/2016/188S1-56561$15.00. All rights reserved. itation throughout the year provide suitable conditions for a DOI: 10.1086/687547 larger number of reproductive modes, whereas sites with low This content downloaded from 129.101.056.053 on September 14, 2017 15:47:44 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). S42 The American Naturalist precipitation and seasonal climates support mostly aquatic neous polyandry because fertilization is external in most reproductive modes or those otherwise specialized to resist species, breeding aggregations are often large, and opera- desiccation (Silva et al. 2012). These analyses support the hy- tional sex ratios (OSR) can be highly skewed in favor of pothesis that abiotic factors, specifically low temperature and males (Kvarnemo and Ahnesjo 1996; Byrne and Roberts humidity, could constrain the evolution of terrestrial repro- 2004). Simultaneous polyandry is likely more common in ductive modes in temperate clades. However, they do not ac- explosive breeders that congregate around ponds and lakes count for the complexity of traits that co-occur with egg and for reproduction and have fully exposed amplexus, because larval development (parental care, courtship, mating systems) a large number of males are actively searching for females or the effects of phylogeny on the combined evolution of (Wells 1977; Chuang et al. 2013), increasing the probability those traits. Focus on the abiotic limitation hypothesis fails that more than one male will try to fertilize a female’s to recognize other selective mechanisms within the highly clutch. The probability of simultaneous polyandry will be variable tropical and temperate environments that contrib- smaller in prolonged breeders that congregate around wa- ute to global diversity of reproductive patterns in frogs. ter bodies at lower densities and will be much smaller in The earliest hypotheses for the evolution of reproductive breeders that do not congregate around water (such as modes focused on a linear evolutionary progression from direct-developing species), in species that actively defend ter- aquatic to increasingly terrestrial eggs and tadpoles, with the ritories or nest sites (Chuang et al. 2013), or in species that assumption that terrestriality enhances fitness due to lower hide from competitors during amplexus (Ovaska and Rand loss of eggs and tadpoles to aquatic predators (Lutz 1947; 2001; Mangold et al. 2015). Our hypothesis is that the selec- Goin and Goin 1962; Heyer 1969). To this day, most analyses tive mechanism driving diversification of reproductive modes of reproductive modes in Anura assume that the main selec- is not simply predation of eggs and tadpoles but that intra- tive regime driving the evolution of terrestrial breeding is the sexual selection, specifically the escape from male-male com- protection of eggs and larvae (Magnusson and Hero 1991; petition for fertilization, also contributes to the observed di- Gomez-Mestre et al. 2012). Although escape from aquatic versification in reproductive modes among frogs. predation has clear benefits (Alford 1999), this hypothesis If, as is generally assumed, escape from aquatic predators assumes that predation of eggs and larvae are significantly is the main selective force driving the evolution of frog re- higher in aquatic than terrestrial environments. Predation productive modes, we would expect that both eggs and lar- on terrestrial eggs, however, is also common (Warkentin vae would evolve in a correlated fashion across the phylog- 2000; Warkentin et al. 2001; Carvalho et al. 2012), and in- eny of frogs. If transitions to increased terrestriality occur creased terrestriality entails additional costs such as desicca- disproportionately in one of those components of repro- tion (Martin 1999; Touchon and Worley 2015), potential re- ductive modes—for example, if across the phylogeny we duction in gas exchange (Seymour et al. 1995; Warkentin et al. see more species variation in egg deposition than in tadpole 2005), limitation of egg-laying and/or nesting sites (Heying sites—then this indicates that the fitness benefits of aquatic 2004; Lin et al. 2008), and the potential need for parental care development potentially differ for those two life-history of terrestrial eggs and larvae. Recent phylogenetic analyses stages. If, as we propose, decreased exposure to simulta- show that aquatic reproduction is ancestral in frogs but that neous polyandry is an important mechanism driving males reproductive traits are labile and complex (Gomez-Mestre to seek