Feral frogs, native newts, and chemical cues: identifying threats from and management opportunities for invasive African Clawed Frogs in Washington state.

Invasive species threaten biodiversity globally. Amphibians are one of the most threatened vertebrate taxa and are particularly sensitive to invasive species, including other amphibians. African clawed frogs (Xenopus laevis) are native to Southern Africa but have subsequently become invasive on multiple continents-including multiple parts of North America-due to releases from the pet and biomedical trades. Despite their prevalence as a global invader, the impact of X. laevis remains understudied. This includes the Pacific Northwest of the USA, which now hosts multiple expanding X. laevis populations. For many amphibians, chemical cues communicate important information, including the presence of predators. Here, we tested the role chemical cues may play in mediating interactions between feral X. laevis and native amphibians in the Pacific Northwest. We tested whether native red-legged frog (Rana aurora) tadpoles display an antipredator response to non-native frog (X. laevis) or native newt (rough-skinned newts, Taricha granulosa) predator chemical stimuli. We found that R. aurora tadpoles exhibited pronounced anti-predator responses when exposed to chemical cues from T. granulosa but did not display anti-predator response to invasive X. laevis chemical cues. We also began experimentally testing whether T. granulosa-which produce a powerful neurotoxin tetrodotoxin (TTX)-may elicit an anti-predator response in X. laevis, that could serve to deter co-occupation. However, our short-duration experiments found that X. laevis were attracted to newt chemical stimuli rather than deterred. Our findings show that X. laevis likely poses a threat to native amphibians, and that these native species may also be particularly vulnerable to this invasive predator, compared to native predators, because toxic native newts may not limit X. laevis invasions. Our research provides some of the first indications that native Pacific Northwest species may be threatened by feral X. laevis and provides a foundation for future experiments testing potential management techniques for X. laevis.

Bacterial communities of the threatened Western Pond Turtle may be impacted by land use.

As semi-aquatic species that use both terrestrial and aquatic habitats, freshwater turtles and their microbial communities are especially sensitive to the impacts of habitat disturbance. In this study, we use 16S rRNA amplicon sequencing to characterize the shell and cloacal bacterial communities of turtles in the San Francisco Bay Area. We captured western pond turtles (Actinemys/Emys marmorata) across eight sites located in urban and rural environments, along with invasive red-eared sliders (Trachemys scripta elegans). We assessed differences in western pond turtle bacterial communities diversity/composition between shell and cloacal samples and evaluated how alpha/beta diversity metrics were influenced by habitat quality. We found phylum-level bacterial taxonomic turnover in the bacterial communities of western pond turtles relative to the host tissue substrate samples. Our findings indicate that location identity elicits a high degree of lower-level (i.e. species/genus) bacterial taxonomic turnover. Further, we found that samples originating from good quality habitat had poorer shell bacterial communities but more diverse cloacal ones. The shell bacterial communities of red-eared sliders overlapped with those western pond turtles suggesting the existence of microbial dispersal between these two species. Our results add to our current understanding of turtle symbiont microbial ecology by establishing patterns of bacterial symbiont variation in an urban to rural gradient.

Relationships between maternally-transferred mercury and hatchling development, behavior, and survival in the American alligator (Alligator mississippiensis).

Mercury is a toxic and pervasive environmental contaminant that can be transferred from mother to offspring during development. Consequences of maternally-transferred mercury have been observed in vertebrate taxa, including reduced clutch viability, reduced offspring size, and behavioral alterations. These sublethal effects have been assumed to decrease survivorship, though this is seldom assessed. Here, we examined how maternally-transferred mercury interacts with incubation temperature to influence reproductive success, offspring behavior, and subsequent survival in the American alligator (Alligator mississippiensis). We collected nine clutches of eggs from a mercury contaminated reservoir on the Savannah River Site, South Carolina, and incubated eggs at either female- or male-promoting temperatures. Clutch-averaged mercury in egg yolk was high relative to other studies in crocodilians and ranged from 0.248 to 0.554 ppm compared to 0.018-0.052 ppm at a site with low levels of mercury contamination; mercury levels in hatchling blood ranged from 0.090 to 0.490 ppm (x¯ = 0.240 ppm, n = 158). We found few, mostly negligible correlations between life history traits and mercury but noted a positive relationship with egg mass, possibly mediated by correlated maternal effects such as resource provisioning. Incubation temperature exerted strong effects on hatchling phenotypes, with warmer, male-promoting temperatures producing larger and bolder hatchlings. Presumptive females, produced from cooler incubation temperatures, spent more time in warm areas during behavior trials. Hatchlings were released 10-15 days post-hatch and surveyed over eight months to assess survival. Survivorship was positively correlated with hatchling size and negatively correlated with proportional time spent in warm areas. Presumptive females had much lower survival, and overall survivorship for the eight-month period was 0.185-0.208, depending on the modelling approach. Our study suggests that, within the range of concentrations we observed, incubation temperature has a stronger effect on offspring behavior and survival than maternally-transferred mercury pollution in American alligators.

Behavioral plasticity can facilitate evolution in urban environments.

Plasticity-led evolution is central to evolutionary theory. Although challenging to study in nature, this process may be particularly apparent in novel environments such as cities. We document abundant evidence of plastic behavioral changes in urban animals, including learning, contextual, developmental, and transgenerational plasticities. Using behavioral drive as a conceptual framework, our analysis of notable case studies suggests that plastic behaviors, such as altered habitat use, migration, diurnal and seasonal activity, and courtship, can have faciliatory and cascading effects on urban evolution via spatial, temporal, and mate-choice mechanisms. Our findings highlight (i) the need to incorporate behavioral plasticity more formally into urban evolutionary research and (ii) the opportunity provided by urban environments to study behavioral mechanisms of plasticity-led processes.

What's Gender Got to Do with It? Dismantling the Human Hierarchies in Evolutionary Biology and Environmental Toxicology for Scientific and Social Progress.

AbstractThis article argues that the concepts of "normal" reproductive development that biologists rely on are undergirded by heterosexism, ableism, and White supremacism, even if implicitly. We illustrate our argument by critically analyzing toxicology's use of reproductive fitness, focusing on the field of endocrine-disrupting chemicals (EDCs). Toxicology both informs and is informed by fundamental evolutionary and ecological questions as well as environmental health. Throughout, biologists overwhelmingly assume that "abnormal" reproductive physiologies both are generated by EDC exposure and necessarily threaten species survival. Such assumptions unwittingly obscure fundamental scientific insights while further discriminating against queer, trans, nonbinary, and differently abled human communities. We agree that scientists should be sounding the alarm over unavoidable, unevenly distributed, highly hazardous EDC exposures-which cause metabolic dysregulation, cancer, and death-but not because gonads and genitals look different. Instead, we encourage scientists to directly confront how chemical corporations profit from innumerable, irreversible harms to ecological and societal well-being, harms that may very well have nothing to do with gonads or genitals. We close with three specific suggestions to help scientists dismantle the human hierarchies embedded in biological frameworks, toward better science and environmental justice. By refusing the oppressive social ideologies assumed by prior research, toxicological and biological scientists will offer exciting new insights into evolutionary processes and urgent, justice-centered findings for environmental health.

Socio-eco-evolutionary dynamics in cities.

Cities are uniquely complex systems regulated by interactions and feedbacks between nature and human society. Characteristics of human society-including culture, economics, technology and politics-underlie social patterns and activity, creating a heterogeneous environment that can influence and be influenced by both ecological and evolutionary processes. Increasing research on urban ecology and evolutionary biology has coincided with growing interest in eco-evolutionary dynamics, which encompasses the interactions and reciprocal feedbacks between evolution and ecology. Research on both urban evolutionary biology and eco-evolutionary dynamics frequently focuses on contemporary evolution of species that have potentially substantial ecological-and even social-significance. Still, little work fully integrates urban evolutionary biology and eco-evolutionary dynamics, and rarely do researchers in either of these fields fully consider the role of human social patterns and processes. Because cities are fundamentally regulated by human activities, are inherently interconnected and are frequently undergoing social and economic transformation, they represent an opportunity for ecologists and evolutionary biologists to study urban "socio-eco-evolutionary dynamics." Through this new framework, we encourage researchers of urban ecology and evolution to fully integrate human social drivers and feedbacks to increase understanding and conservation of ecosystems, their functions and their contributions to people within and outside cities.

Adaptive Evolution in Cities: Progress and Misconceptions.

Current narratives suggest that urban adaptation - the adaptive evolution of organisms to cities - is pervasive across taxa and cities. However, in reviewing hundreds of studies, we find only six comprehensive examples of species adaptively evolving to urbanization. We discuss the utility and shortcomings of methods for studying urban adaptation. We then review diverse systems offering preliminary evidence for urban adaptation and outline a research program for advancing its study. Urban environments constitute diverse, interacting selective agents that test the limits of adaptation. Understanding urban adaptation therefore offers unique opportunities for addressing fundamental questions in evolutionary biology and for better conserving biodiversity in cities. However, capitalizing on these opportunities requires appropriate research methods and dissemination of accurate narratives.

The ecological and evolutionary consequences of systemic racism in urban environments.

Urban areas are dynamic ecological systems defined by interdependent biological, physical, and social components. The emergent structure and heterogeneity of urban landscapes drives biotic outcomes in these areas, and such spatial patterns are often attributed to the unequal stratification of wealth and power in human societies. Despite these patterns, few studies have effectively considered structural inequalities as drivers of ecological and evolutionary outcomes and have instead focused on indicator variables such as neighborhood wealth. In this analysis, we explicitly integrate ecology, evolution, and social processes to emphasize the relationships that bind social inequities-specifically racism-and biological change in urbanized landscapes. We draw on existing research to link racist practices, including residential segregation, to the heterogeneous patterns of flora and fauna observed by urban ecologists. In the future, urban ecology and evolution researchers must consider how systems of racial oppression affect the environmental factors that drive biological change in cities. Conceptual integration of the social and ecological sciences has amassed considerable scholarship in urban ecology over the past few decades, providing a solid foundation for incorporating environmental justice scholarship into urban ecological and evolutionary research. Such an undertaking is necessary to deconstruct urbanization's biophysical patterns and processes, inform equitable and anti-racist initiatives promoting justice in urban conservation, and strengthen community resilience to global environmental change.

Urban biodiversity management using evolutionary tools.

Cities are fully functioning ecosystems and are home to no-analogue communities of species that interact with each other and which are subject to novel urban stressors. As such, biodiversity can evolve in response to these new urban conditions, making urban species a moving target for conservation and management efforts. An evolving urban biodiversity necessitates integrating evolutionary insights into management for these efforts to be successful in a dynamic urban milieu. Here we present a framework for categorizing urban biodiversity from a management perspective. We then discuss a suite of example management tools and their potential evolutionary implications-both their opportunities for and potential consequence to management. Urban ecosystems are proliferating but, far from being ecological lost causes, they may provide unique insights and opportunities for biodiversity conservation. Determining how to achieve urban biodiversity priorities while managing pest species requires evolutionary thinking.

Comment on "Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity".

Scheele et al (Reports, 29 March 2019, p. 1459) bring needed attention to the effects of amphibian infectious disease. However, the data and methods implicating the disease chytridiomycosis in 501 amphibian species declines are deficient. Which species are affected, and how many, remains a critical unanswered question. Amphibians are imperiled; protective actions require public support and robust science.

Author Correction: An alternative hypothesis for the evolution of same-sex sexual behaviour in animals.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

An alternative hypothesis for the evolution of same-sex sexual behaviour in animals.

Same-sex sexual behaviour (SSB) has been recorded in over 1,500 animal species with a widespread distribution across most major clades. Evolutionary biologists have long sought to uncover the adaptive origins of 'homosexual behaviour' in an attempt to resolve this apparent Darwinian paradox: how has SSB repeatedly evolved and persisted despite its presumed fitness costs? This question implicitly assumes that 'heterosexual' or exclusive different-sex sexual behaviour (DSB) is the baseline condition for animals, from which SSB has evolved. We question the idea that SSB necessarily presents an evolutionary conundrum, and suggest that the literature includes unchecked assumptions regarding the costs, benefits and origins of SSB. Instead, we offer an alternative null hypothesis for the evolutionary origin of SSB that, through a subtle shift in perspective, moves away from the expectation that the origin and maintenance of SSB is a problem in need of a solution. We argue that the frequently implicit assumption of DSB as ancestral has not been rigorously examined, and instead hypothesize an ancestral condition of indiscriminate sexual behaviours directed towards all sexes. By shifting the lens through which we study animal sexual behaviour, we can more fruitfully examine the evolutionary history of diverse sexual strategies.

Two salamander species respond differently to timber harvests in a managed New England forest.

BACKGROUND: Managing forests for timber while protecting wildlife habitat is of increasing concern. Amphibians may be particularly sensitive to forest management practices due to their unique biology; however, it is not clear how different species respond to timber harvest practices-particularly over longer time scales. METHODS: Here we report on the differential responses of two salamander species-the eastern red-backed salamander (Plethodon cinereus Green) and the eastern newt (Notophthalmus viridescens Rafinesque)-to forest harvesting, by examining communities across a 25-year chronosequence of regenerating shelterwood harvests. RESULTS: Populations of both species were lowest immediately after harvest, but increased at substantially different rates. Red-backed salamander populations were highest in 20-25 year-old shelterwoods-significantly higher than in mature, unharvested, control (100-120 year old) stands. Eastern newt populations, however, were greatest in unharvested control stands and still had not recovered to population levels found in mature stands in the 25 years since harvest. Red-backed salamander abundances were strongly tied to stand age as well as abundance of decayed coarse woody debris, suggesting that timber harvests influence some wildlife species by affecting a suite of interacting habitat variables that change over time. In contrast, newt abundances were not directly related to stand age but were more related to downed wood and vegetation characteristics. Our results highlight markedly variable responses by two common salamander species to forest harvesting-species with markedly different life histories and reproductive patterns-and that time since harvest may be useful in predicting abundance.

Experimental removal of introduced slider turtles offers new insight into competition with a native, threatened turtle.

The red-eared slider turtle (Trachemys scripta elegans; RES) is often considered one of the world's most invasive species. Results from laboratory and mesocosm experiments suggest that introduced RES outcompete native turtles for key ecological resources, but such experiments can overestimate the strength of competition. We report on the first field experiment with a wild turtle community, involving introduced RES and a declining native species of conservation concern, the western pond turtle (Emys marmorata; WPT). Using a before/after experimental design, we show that after removing most of an introduced RES population, the remaining RES dramatically shifted their spatial basking distribution in a manner consistent with strong intraspecific competition. WPT also altered their spatial basking distribution after the RES removal, but in ways inconsistent with strong interspecific competition. However, we documented reduced levels of WPT basking post-removal, which may reflect a behavioral shift attributable to the lower density of the turtle community. WPT body condition also increased after we removed RES, consistent with either indirect or direct competition between WPT and RES and providing the first evidence that RES can compete with a native turtle in the wild. We conclude that the negative impacts on WPT basking by RES in natural contexts are more limited than suggested by experiments with captive turtles, although wild WPT do appear to compete for food with introduced RES. Our results highlight the importance of manipulative field experiments when studying biological invasions, and the potential value of RES removal as a management strategy for WPT.

Suburbanization Increases Echinostome Infection in Green Frogs and Snails.

An important contribution to infectious disease emergence in wildlife is environmental degradation driven by pollution, habitat fragmentation, and eutrophication. Amphibians are a wildlife group that is particularly sensitive to land use change, infectious diseases, and their interactions. Residential suburban land use is now a dominant, and increasing, form of land cover in the USA and globally, contributing to increased pollutant and nutrient loading in freshwater systems. We examined how suburbanization affects the infection of green frog (Rana clamitans) tadpoles and metamorphs by parasitic flatworms (Echinostoma spp.) through the alteration of landscapes surrounding ponds and concomitant changes in water quality. Using sixteen small ponds along a forest-suburban land use gradient, we assessed how the extent of suburban land use surrounding ponds influenced echinostome infection in both primary snail and secondary frog hosts. Our results show that the degree of suburbanization and concurrent chemical loading are positively associated with the presence and burden of echinostome infection in both host populations. This work contributes to a broader understanding of how land use mediates wildlife parasitism and shows how human activities at the household scale can have similar consequences for wildlife health as seemingly more intensive land uses like agriculture or urbanization.

Molecular evidence for sex reversal in wild populations of green frogs (Rana clamitans).

In vertebrates, sex determination occurs along a continuum from strictly genotypic (GSD), where sex is entirely guided by genes, to strictly environmental (ESD), where rearing conditions, like temperature, determine phenotypic sex. Along this continuum are taxa which have combined genetic and environmental contributions to sex determination (GSD + EE), where some individuals experience environmental effects which cause them to sex reverse and develop their phenotypic sex opposite their genotypic sex. Amphibians are often assumed to be strictly GSD with sex reversal typically considered abnormal. Despite calls to understand the relative natural and anthropogenic causes of amphibian sex reversal, sex reversal has not been closely studied across populations of any wild amphibian, particularly in contrasting environmental conditions. Here, we use sex-linked molecular markers to discover sex reversal in wild populations of green frogs (Rana clamitans) inhabiting ponds in either undeveloped, forested landscapes or in suburban neighborhoods. Our work here begins to suggest that sex reversal may be common within and across green frog populations, occurring in 12 of 16 populations and with frequencies of 2-16% of individuals sampled within populations. Additionally, our results also suggest that intersex phenotypic males and sex reversal are not correlated with each other and are also not correlated with suburban land use. While sex reversal and intersex are often considered aberrant responses to human activities and associated pollution, we found no such associations here. Our data perhaps begin to suggest that, relative to what is often suggested, sex reversal may be a relatively natural process in amphibians. Future research should focus on assessing interactions between genes and the environment to understand the molecular and exogenous basis of sex determination in green frogs and in other amphibians.

Sexual and somatic development of wood frog tadpoles along a thermal gradient.

All amphibian species are known to have genetic sex determination. However, a variety of environmental conditions can moderate sexual differentiation, in some cases leading to sex reversal and skewed sex ratios. While there has been a recent focus on chemically-induced sex reversal in amphibians, temperature can also influence sexual differentiation. Building upon a classic 1929 study by Emil Witschi, we assessed temperature-mediated sex reversal. Witschi found that the wood frog sex ratio is 100% male at a high temperature (32°C) compared to a 50:50 sex ratio at 20°C. This pattern is consistent with multiple models of environmentally mediated sexual differentiation in vertebrates. To better understand thermally mediated sex reversal, we raised wood frogs at temperature increments of ∼1°C between 19 and 34°C. Mirroring earlier findings, wood frog metamorph sex ratios are indistinguishable from 50:50 at the lowest temperature and entirely male at the highest temperatures. In between, sex ratios become increasingly male-dominated as temperatures increase, implying a steadily increasing tendency toward female-to-male sex reversal in warmer environments. There was no evidence of a threshold temperature effect on reversal patterns. We also show that, compared to males, females metamorphose larger and later in cooler conditions but earlier and smaller under warmer conditions. While the ecological relevance in this species is unknown, these results conform to the Charnov-Bull model of sex determination (in which female-to-male sex reversal can increase fitness to genetic females at higher temperatures), suggesting the system would reward further study.

Hormonally active phytochemicals and vertebrate evolution.

Living plants produce a diversity of chemicals that share structural and functional properties with vertebrate hormones. Wildlife species interact with these chemicals either through consumption of plant materials or aquatic exposure. Accumulating evidence shows that exposure to these hormonally active phytochemicals (HAPs) often has consequences for behavior, physiology, and fecundity. These fitness effects suggest there is potential for an evolutionary response by vertebrates to HAPs. Here, we explore the toxicological HAP-vertebrate relationship in an evolutionary framework and discuss the potential for vertebrates to adapt to or even co-opt the effects of plant-derived chemicals that influence fitness. We lay out several hypotheses about HAPs and provide a path forward to test whether plant-derived chemicals influence vertebrate reproduction and evolution. Studies of phytochemicals with direct impacts on vertebrate reproduction provide an obvious and compelling system for studying evolutionary toxicology. Furthermore, an understanding of whether animal populations evolve in response to HAPs could provide insightful context for the study of rapid evolution and how animals cope with chemical agents in the environment.