Polyphenism predicts actuarial senescence and lifespan in tiger salamanders.

Actuarial senescence (called 'senescence' hereafter) often shows broad variation at the intraspecific level. Phenotypic plasticity likely plays a central role in among-individual heterogeneity in senescence rate (i.e. the rate of increase in mortality with age), although our knowledge on this subject is still very fragmentary. Polyphenism-the unique sub-type of phenotypic plasticity where several discrete phenotypes are produced by the same genotype-may provide excellent study systems to investigate if and how plasticity affects the rate of senescence in nature. In this study, we investigated whether facultative paedomorphosis influences the rate of senescence in a salamander, Ambystoma mavortium nebulosum. Facultative paedomorphosis, a unique form of polyphenism found in dozens of urodele species worldwide, leads to the production of two discrete, environmentally induced phenotypes: metamorphic and paedomorphic individuals. We leveraged an extensive set of capture-recapture data (8948 individuals, 24 years of monitoring) that were analysed using multistate capture-recapture models and Bayesian age-dependent survival models. Multistate models revealed that paedomorphosis was the most common developmental pathway used by salamanders in our study system. Bayesian age-dependent survival models then showed that paedomorphs have accelerated senescence in both sexes and shorter adult lifespan (in females only) compared to metamorphs. In paedomorphs, senescence rate and adult lifespan also varied among ponds and individuals. Females with good body condition and high lifetime reproductive success had slower senescence and longer lifespan. Late-breeding females also lived longer but showed a senescence rate similar to that of early-breeding females. Moreover, males with good condition had longer lifespan than males with poor body condition, although they had similar senescence rates. In addition, late-breeding males lived longer but, unexpectedly, had higher senescence than early-breeding males. Overall, our work provides one of the few empirical cases suggesting that environmentally cued polyphenism could affect the senescence of a vertebrate in nature, thus providing insights on the ecological and evolutionary consequences of developmental plasticity on ageing.

Simulated climate warming causes asymmetric responses in insect life-history timing potentially disrupting a classic ecological speciation system.

Climate change may alter phenology within populations with cascading consequences for community interactions and on-going evolutionary processes. Here, we measured the response to climate warming in two sympatric, recently diverged (~170 years) populations of Rhagoletis pomonella flies specialized on different host fruits (hawthorn and apple) and their parasitoid wasp communities. We tested whether warmer temperatures affect dormancy regulation and its consequences for synchrony across trophic levels and temporal isolation between divergent populations. Under warmer temperatures, both fly populations developed earlier. However, warming significantly increased the proportion of maladaptive pre-winter development in apple, but not hawthorn, flies. Parasitoid phenology was less affected, potentially generating ecological asynchrony. Observed shifts in fly phenology under warming may decrease temporal isolation, potentially limiting on-going divergence. Our findings of complex sensitivity of life-history timing to changing temperatures predict that coming decades may see multifaceted ecological and evolutionary changes in temporal specialist communities.

The role of sexual isolation during rapid ecological divergence: Evidence for a new dimension of isolation in Rhagoletis pomonella.

The pace of divergence and likelihood of speciation often depends on how and when different types of reproductive barriers evolve. Questions remain about how reproductive isolation evolves after initial divergence. We tested for the presence of sexual isolation (reduced mating between populations due to divergent mating preferences and traits) in Rhagoletis pomonella flies, a model system for incipient ecological speciation. We measured the strength of sexual isolation between two very recently diverged (~170 generations) sympatric populations, adapted to different host fruits (hawthorn and apple). We found that flies from both populations were more likely to mate within than between populations. Thus, sexual isolation may play an important role in reducing gene flow allowed by early-acting ecological barriers. We also tested how warmer temperatures predicted under climate change could alter sexual isolation and found that sexual isolation was markedly asymmetric under warmer temperatures - apple males and hawthorn females mated randomly while apple females and hawthorn males mated more within populations than between. Our findings provide a window into the early speciation process and the role of sexual isolation after initial ecological divergence, in addition to examining how environmental conditions could shape the likelihood of further divergence.

The role of environmental variation in mediating fitness trade-offs for an amphibian polyphenism.

Fitness trade-offs are a foundation of ecological and evolutionary theory because trade-offs can explain life history variation, phenotypic plasticity, and the existence of polyphenisms. Using a 32-year mark-recapture dataset on lifetime fitness for 1093 adult Arizona tiger salamanders (Ambystoma mavortium nebulosum) from a high elevation, polyphenic population, we evaluated the extent to which two life history morphs (aquatic paedomorphs vs. terrestrial metamorphs) exhibited fitness trade-offs in breeding and body condition with respect to environmental variation (e.g. climate) and internal state-based variables (e.g. age). Both morphs displayed a similar response to higher probabilities of breeding during years of high spring precipitation (i.e. not indicative of a morph-specific fitness trade-off). There were likely no climate-induced fitness trade-offs on breeding state for the two life history morphs because precipitation and water availability are vital to amphibian reproduction. Body condition displayed a contrasting response for the two morphs that was indicative of a climate-induced fitness trade-off. While metamorphs exhibited a positive relationship with summer snowpack conditions, paedomorphs were unaffected. Fitness trade-offs from summer snowpack are likely due to extended hydroperiods in temporary ponds, where metamorphs gain a fitness advantage during the summer growing season by exploiting resources that are unavailable to paeodomorphs. However, paedomorphs appear to have the overwintering fitness advantage because they consistently had higher body condition than metamorphs at the start of the summer growing season. Our results reveal that climate and habitat type (metamorphs as predominately terrestrial, paedomorphs as fully aquatic) interact to confer different advantages for each morph. These results advance our current understanding of fitness trade-offs in this well-studied polyphenic amphibian by integrating climate-based mechanisms. Our conclusions prompt future studies to explore how climatic variation can maintain polyphenisms and promote life history diversity, as well as the implications of climate change for polyphenisms.

Lifetime Fitness, Sex-Specific Life History, and the Maintenance of a Polyphenism.

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.

Experimental warming reduces body mass but not reproductive investment.

Climate change has already had wide-ranging effects on populations, including shifts in species' ranges, phenology, and body size. Whereas some common patterns have emerged, the direction and magnitude of responses vary extensively among populations as well as across life stages within populations. Understanding the consequences of climate change and predicting future responses at the population level require experimental tests of how warmer temperatures affect life history traits, including growth rate, development time, and reproductive output. Here, we tested how experimental warming affected life history from larval development and survival to adult reproductive maturity and investment in mole salamanders, Ambystoma talpoideum. We found that a small temperature increase (~1°C) experienced during larval development had complex consequences: density-dependent effects on growth and body mass, density-independent effects on fat storage, and no effects on survival and reproductive investment. Although warming reduced growth rates, size at maturity, and fat storage, salamanders in both warmed and control conditions had similar survival and reproductive investment in their first year. However, costs of smaller body size and lower fat reserves may limit overwintering survival and/or future reproduction. Our study highlights the differential effects of warming across life history traits and multifaceted population responses to climate change. This work motivates future studies to examine variation in response to climate change across life stages and life history traits.

Expanding the landscape of opportunity: Professional societies support early-career researchers through community programming and peer coaching.

Weaving the future of the field of comparative psychology is dependent on the career advancement of early-career scientists. Despite concerted efforts to increase diversity in science, technology, engineering, and mathematics, scholars from marginalized groups are disproportionately underrepresented in the field-especially at advanced career stages. New approaches to sponsorship, mentoring, and community building are necessary to retain talent from marginalized communities and to create a culture and a system where all individuals can thrive. We describe the unique and supportive role of senior women scientists united through a professional society in initiating peer coaching circles to facilitate the success of a diverse cohort of early-career women scientists. We offer our experiences with the Weaving the Future of Animal Behavior program as a case study that illustrates the cascading impacts of professional societies investing in the success and career development of marginalized scholars. We focus on our peer coaching circle experience and share the products and outcomes after 2 years of meeting. Peer coaching transformed us from a group of loosely organized, anxious individuals into a collective of empowered agents of change with an enhanced sense of belonging. We end by presenting recommendations to institutions seeking to expand the landscape of opportunities to other marginalized scholars. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

The ecological stage changes benefits of mate choice and drives preference divergence.

Preference divergence is thought to contribute to reproductive isolation. Ecology can alter the way selection acts on female preferences, making them most likely to diverge when ecological conditions vary among populations. We present a novel mechanism for ecologically dependent sexual selection, termed 'the ecological stage' to highlight its ecological dependence. Our hypothesized mechanism emphasizes that males and females interact over mating in a specific ecological context, and different ecological conditions change the costs and benefits of mating interactions, selecting for different preferences in distinct environments and different male traits, especially when traits are condition dependent. We test key predictions of this mechanism in a sympatric three-spine stickleback species pair. We used a maternal half-sib split-clutch design for both species, mating females to attractive and unattractive males and raising progeny on alternate diets that mimic the specialized diets of the species in nature. We estimated the benefits of mate choice for an indicator trait (male nuptial colour) by measuring many fitness components across the lifetimes of both sons and daughters from these crosses. We analysed fitness data using a combination of aster and mixed models. We found that many benefits of mating with high-colour males depended on both species and diet. These results support the ecological stage hypothesis for sticklebacks. Finally, we discuss the potential role of this mechanism for other taxa and highlight its ability to enhance reproductive isolation as speciation proceeds, thus facilitating the evolution of strong reproductive isolation. This article is part of the theme issue 'Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.

Evolution of reproductive isolation in stickleback fish.

To understand how new species form and what causes their collapse, we examined how reproductive isolation evolves during the speciation process, considering species pairs with little to extensive divergence, including a recently collapsed pair. We estimated many reproductive barriers in each of five sets of stickleback fish species pairs using our own data and decades of previous work. We found that the types of barriers important early in the speciation process differ from those important late. Two premating barriers-habitat and sexual isolation-evolve early in divergence and remain two of the strongest barriers throughout speciation. Premating isolation evolves before postmating isolation, and extrinsic isolation is far stronger than intrinsic. Completing speciation, however, may require postmating intrinsic incompatibilities. Reverse speciation in one species pair was characterized by significant loss of sexual isolation. We present estimates of barrier strengths before and after collapse of a species pair; such detail regarding the loss of isolation has never before been documented. Additionally, despite significant asymmetries in individual barriers, which can limit speciation, total isolation was essentially symmetric between species. Our study provides important insight into the order of barrier evolution and the relative importance of isolating barriers during speciation and tests fundamental predictions of ecological speciation.