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Summers2007 Social and environmental influences on egg size evolution in frogs

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Social and environmental influences on egg size evolutionin frogsK. Summers1, C. S. McKeon2, H. Heying3, J. Hall1& W. Patrick11 Department of Biology, East Carolina University, Greenville, NC, USA2 Department of Zoology, University of Florida, Gainesville, FL, USA3 The Evergreen State College, Olympia, WA, USAKeywordsparental care; egg size; anurans; phylogeneticsupertree; pairwise comparisons.CorrespondenceKyle Summers, Department of Biology, EastCarolina University, Greenville, NC 27858,USA. Tel: 252 328 6304Email: [email protected] 14 November 2005; accepted17 May 2006doi:10.1111/j.1469-7998.2006.00213.xAbstractThe reproductive strategies of frogs are highly diverse, but analysis of thesestrategies in a phylogenetic context has lagged behind other taxa. Here weinvestigate associations between aspects of parental care and egg size in aphylogenetic context. We obtained data on egg size and parental care strategies invarious species of frogs from the scientific literature. We developed a phylogeneticsupertree of frogs by combining the results of multiple phylogenetic analyses usingmatrix representation parsimony. We used phylogenetic pairwise comparisons toinvestigate the correlation between various forms of parental care and egg sizeacross the order Anura. We also investigated correlations between tadpolecarnivory and egg size, and phytotelm breeding and egg size. We also investigatedthe association of egg size with several environmental factors. Parental care, maleparental care, direct development, stream breeding and montane breeding habitatswere all associated with large egg size. Female care (in species with trophic eggfeeding), carnivory, use of small pools (phytotelmata) and use of temporary poolswere not associated with egg size.IntroductionTheory and data indicate that parental care is likely to affectegg size and number in amphibians and other animals (e.g.Shine, 1978; Nussbaum & Schultz, 1989; Clutton-Brock,1991). Ecological factors are also likely to affect egg andclutch size (Nussbaum, 1985; Stearns, 1992; Morrison &Hero, 2003). Frogs, which display an extraordinary diversityof reproductive strategies (Duellman & Trueb, 1986), are anexcellent taxonomic assemblage in which to investigate therelationships between parental care, ecology and egg size inan evolutionary context.Reproductive diversity in anurans is associated with aspectrum of parental behaviors, the primary aim of which isremoving eggs or tadpoles from large bodies of water, such asponds, to smaller pools or terrestrial sites (Magnusson & Hero,1991). These behaviors include the production of foam nests,the construction of burrows and the use of phytotelmata (smallpools that form in plant structures, such as bromeliad tanks).Many researchers have inves tigated these strategies (e.g.Crump, 1974; Resetarits & Wilbur, 1989; Caldwell & Arau´ jo,1998), and there have been several major reviews (e.g. Salthe &Duellman, 1973; Duellman & Trueb, 1986). Nevertheless, thereis a dearth of investigations of the evolution of frog reproduc-tive strategies using comparative methods that control forphylogenetic effects (e.g. Beck, 1998). In contrast, the use ofphylogenetic trees to inform comparative analyses statisticallyhas become the rule rather than the exception in many othertaxa (e.g. Garland, Huey & Bennett, 1991; Balshine et al., 2001;Liker, Reynolds & Szekely, 2001; Bennett & Owens, 2002).Until very recently there were few well-supported phylo-genies available for frogs, making phylogenetically con-trolled comparative analyses difficult or impossible. Therecent flood of molecular phylogenetic analyses has changedthings dramatically over the last 10 years, yielding robustphylogenetic hypotheses for many clades of frogs. Here weutilize a phylogenetic supertree for several hundred speciesof frogs, which was developed by combining the results of anumber of recent molecular phylogenetic analyses. We thenuse this tree to analyze the relationship between egg size andparental care, as well as other aspects of anuran ecology.Previous studies have investigated various aspects of bothegg and clutch size in the context of reproductive strategiesin frogs (e.g. Salthe & Duellman, 1973; Crump, 1974;Kuramoto, 1978). There has also been considerable debatein the literature concerning the relationship between egg sizeand parental care (Shine, 1978; Nussbaum & Schultz, 1989).Some comparative analyses have indicated that egg sizeincreases in the presence of parental care (e.g. Crump,1995, 1996). However, none of the studies to date havetaken phylogeny into account, calling the statistical validityof any conclusions into question (Harvey & Pagel, 1991).In a previous study (Summers, McKeon & Heying, 2006)we carried out a comparative analysis of parental care andJournal of Zoology 271 (2007) 225–232c2007 The Authors. Journal compilationc2007 The Zoological Society of London 225Journal of Zoology. Print ISSN 0952-8369egg size using the phylogenetic supertree mentioned above.That study dealt specifically with several general hypothesesfor the evolution of egg size: particularly Shine’s (1978) ‘safeharbor hypothesis’ and Nussbaum’s (1985, 1987) hypothesisconcerning the effect of ecological selection on juveniles.The focus of the paper was to use Pagel’s maximum-likelihood method for discrete characters (Pagel, 1994,1997, 1999a,b) to investigate the order of transitions be-tween parental care and egg size (Shine and Nussbaum’shypotheses make opposite predictions in this regard). Theresults of the comparative analysis suggested that, in gen-eral, the evolution of large egg size tends to precede theevolution of parental care, rather than the reverse, althoughthe evolution of parental care does appear to facilitate theevolution of large egg size.Our previous study focused on these general hypothesesconcerning the evolution of parental care and egg size, anddid not subdivide parental care into different types. Thatstudy also did not deal with the effect of ecological factorsthat have been proposed to affect egg size in frogs. Theimportance of ecological factors in driving large egg size wasstressed by Nussbaum (1985, 1987), and our previous studysupporting a prediction of his hypothesis emphasizes theneed for further investigation of the ecological factorsinfluencing egg size. In this study, we use phylogeneticpairwise comparisons to investigate different forms of careseparately (e.g. male vs. female care). We


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