American Society of Naturalists

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“Lifetime fitness, sex-specific life history, and the maintenance of a polyphenism”

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Alycia C. R. Lackey, Michael P. Moore, Jacqueline Doyle, Nicole Gerlanc, Ashley Hagan, Morgan Geile, Chris Eden, and Howard H. Whiteman (Aug 2019)

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Long-term data (27 years) reveals lifetime fitness differs between the sexes of each morph of tiger salamanders

Alternative lifestyles: differences between morphs and sexes in lifetime reproduction help maintain variation within a population

Two morphs of tiger salamanders (<i>Ambystoma mavortium nebulosum</i>): the terrestrial metamorph (top) and aquatic paedomorph (bottom).<br />(Credit: Howard H. Whiteman)
Two morphs of tiger salamanders (Ambystoma mavortium nebulosum): the terrestrial metamorph (top) and aquatic paedomorph (bottom).
(Credit: Howard H. Whiteman)

Studying survival and reproduction within populations provides windows into the processes and mechanisms that underlie the evolutionary origins and maintenance of diversity. Lackey et al. examine a striking type of variation within some salamander populations where a larva can develop into one of two morphs based on its body size and competition: one morph undergoes metamorphosis to become a terrestrial adult, whereas the other retains its larval characteristics and matures as an aquatic adult. While these morphs have long fascinated evolutionary biologists, even gracing the cover of Gould’s landmark Ontogeny and Phylogeny (1977), long-term studies of lifetime costs and benefits are necessary to determine which factors promote the maintenance of two morphs within the same population. Howard Whiteman spearheaded an ongoing long-term research program in 1990 in a population of Arizona Tiger Salamanders in the Rocky Mountains of Colorado. Lackey et al. use 27 years of data from this population to test for differences between each morph and sex in (1) lifetime reproduction, (2) timing of development and reproduction, and (3) consequences of environmental variation across time and space. The authors find that males of the aquatic morph and females of the terrestrial morph have higher lifetime reproduction than the other morph-sex combinations. Thus, sex-specific payoffs likely contribute to maintaining the two morphs in this population. Intriguingly, the morphs achieve these outcomes via different developmental and reproductive strategies. Although the environment shapes which morph a larva becomes, it seems to have little effect on differences between morphs in lifetime reproduction. These results demonstrate how differences in lifetime reproduction can contribute to maintaining trait variation within a population and emphasize the importance of studying reproductive differences between the sexes.


Abstract

Polyphenisms, alternative morphs produced through plasticity, can reveal the evolutionary and ecological processes that initiate and maintain diversity within populations. We examined lifetime fitness consequences of two morphs in a polyphenic population of Arizona Tiger Salamanders using a 27-year data set with 1,317 adults and 6,862 captures across eight generations. Larval salamanders develop into either an aquatic paedomorph that retains larval traits and stays in its natal pond or a terrestrial metamorph that undergoes metamorphosis. To evaluate the adaptive significance of this polyphenism, we compared lifetime reproductive success of each morph and assessed how life history strategies and spatiotemporal variation explained fitness. We found sex-specific differences in lifetime fitness between morphs. For males, paedomorphs had more reproductive opportunities than metamorphs when we accounted for the potential mating advantage of larger males. For females, in contrast, metamorphs had higher estimated egg production than paedomorphs. Life history strategies differed between morphs largely because the morphs maximized different ends of the trade-off between age at first reproduction and longevity. Spatiotemporal variation affected larval more than adult life history traits with little to no effect on lifetime fitness. Thus, environmental variation likely explains differences in morph production across time and space but contributes little to lifetime fitness differences between morphs and sexes. Our long-term study and measures of lifetime fitness provide unique insight into the complex selective regimes potentially acting on each morph and sex. Our findings motivate future work to examine how sex-specific selection may contribute to the maintenance of polyphenism.