Is the future female for turtles? Climate change and wetland configuration predict sex ratios of a freshwater species.

Climate change and land-use change are leading drivers of biodiversity decline, affecting demographic parameters that are important for population persistence. For example, scientists have speculated for decades that climate change may skew adult sex ratios in taxa that express temperature-dependent sex determination (TSD), but limited evidence exists that this phenomenon is occurring in natural settings. For species that are vulnerable to anthropogenic land-use practices, differential mortality among sexes may also skew sex ratios. We sampled the spotted turtle (Clemmys guttata), a freshwater species with TSD, across a large portion of its geographic range (Florida to Maine), to assess the environmental factors influencing adult sex ratios. We present evidence that suggests recent climate change has potentially skewed the adult sex ratio of spotted turtles, with samples following a pattern of increased proportions of females concomitant with warming trends, but only within the warmer areas sampled. At intermediate temperatures, there was no relationship with climate, while in the cooler areas we found the opposite pattern, with samples becoming more male biased with increasing temperatures. These patterns might be explained in part by variation in relative adaptive capacity via phenotypic plasticity in nest site selection. Our findings also suggest that spotted turtles have a context-dependent and multi-scale relationship with land use. We observed a negative relationship between male proportion and the amount of crop cover (within 300 m) when wetlands were less spatially aggregated. However, when wetlands were aggregated, sex ratios remained consistent. This pattern may reflect sex-specific patterns in movement that render males more vulnerable to mortality from agricultural machinery and other threats. Our findings highlight the complexity of species' responses to both climate change and land use, and emphasize the role that landscape structure can play in shaping wildlife population demographics.

Density-dependent fitness, not dispersal movements, drives temporal variation in spatial genetic structure in dark-eyed juncos (Junco hyemalis).

Some studies have found that dispersal rates and distances increase with density, indicating that density-dependent dispersal likely affects spatial genetic structure. In an 11-year mark-recapture study on a passerine, the dark-eyed junco, we tested whether density affected dispersal distance and/or fine-scale spatial genetic structure. Contrary to expectations, we found no effect of predispersal density on dispersal distance or the proportion of locally produced juveniles returning to the population from which they hatched. However, even though density did not affect dispersal distance or natal return rates, we found that density still did affect spatial genetic structure. We found significant positive spatial genetic structure at low densities of (postdispersal) adults but not at high densities. In years with high postdispersal (adult) densities that also had high predispersal (juvenile) densities in the previous year, we found negative spatial genetic structure, indicating high levels of dispersal. We found that density also affected fitness of recruits, and fitness of immigrants, potentially linking these population parameters with the spatial genetic structure detected. Immigrants and recruits rarely nested in low postdispersal density years. In contrast, in years with high postdispersal density, recruits were common and immigrants had equal success to local birds, so novel genotypes diluted the gene pool and effectively eliminated positive spatial genetic structure. In relation to fine-scale spatial genetic structure, fitness of immigrants and new recruits is poorly understood compared to dispersal movements, but we conclude that it can have implications for the spatial distribution of genotypes in populations.

Color-Biased Dispersal Inferred by Fine-Scale Genetic Spatial Autocorrelation in a Color Polymorphic Salamander.

Behavioral traits can be influenced by predation rates of color morphs, potentially leading to reduced boldness or increased escape behaviors in one color morph. The red-backed salamander, Plethodon cinereus, is a small terrestrial salamander whose color morphs have different diets and select different microhabitats, but little is known about potential differences in dispersal behaviors. We used fine-scale genetic spatial autocorrelation to examine 122 P. cinereus in a color-polymorphic population at 10 microsatellite loci in order to generate estimates of spatial genetic structure for each color morph. Differences in spatial genetic structure have been used extensively to infer within-population sex-biased dispersal but have never been used to test for dispersal differences between other groups within populations such as color morphs. We found evidence for color-biased dispersal, but not sex-biased dispersal. Striped salamanders had significant positive genetic structure in the shortest distance classes indicating philopatry. In contrast, unstriped salamanders showed a lack of spatial genetic structure at shorter distances and higher than expected genetic similarity at further distances, as expected if they are dispersing from their natal site. These results show that genetic methods typically used for sex-biased dispersal can be used to investigate differences in dispersal between morphs that vary discretely in polymorphic populations, such as color morphs.

Similarity in temporal variation in sex-biased dispersal over short and long distances in the dark-eyed junco, Junco hyemalis.

Patterns of sex-biased dispersal (SBD) are typically consistent within taxa, for example female-biased in birds and male-biased in mammals, leading to theories about the evolutionary pressures that lead to SBD. However, generalizations about the evolution of sex biases tend to overlook that dispersal is mediated by ecological factors that vary over time. We examined potential temporal variation in between- and within-population dispersal over an 11-year period in a bird, the dark-eyed junco (Junco hyemalis). We measured between-population dispersal patterns using genetic assignment indices and found yearly variation in which sex was more likely to have immigrated. When we measured within-population spatial genetic structure and mark­recapture dispersal distances, we typically found yearly SBD patterns that mirrored between-population dispersal, indicating common eco-evolutionary causes despite expected differences due to the scale of dispersal. However, in years without detectable between-population sex biases, we found genetic similarity between nearby males within our population. This suggests that, in certain circumstances, ecological pressures may act on within-population dispersal without affecting dispersal between populations. Alternatively, current analytical tools may be better able to detect within-population SBD. Future work will investigate potential causes of the observed temporal variation in dispersal patterns and whether they have greater effects on within-population dispersal.

(Not) far from home: No sex bias in dispersal, but limited genetic patch size, in an endangered species, the Spotted Turtle (Clemmys guttata).

Sex-biased dispersal is common in many animals, with male-biased dispersal often found in studies of mammals and reptiles, including interpretations of spatial genetic structure, ostensibly as a result of male-male competition and a lack of male parental care. Few studies of sex-biased dispersal have been conducted in turtles, but a handful of studies, in saltwater turtles and in terrestrial turtles, have detected male-biased dispersal as expected. We tested for sex-biased dispersal in the endangered freshwater turtle, the spotted turtle (Clemmys guttata) by investigating fine-scale genetic spatial structure of males and females. We found significant spatial genetic structure in both sexes, but the patterns mimicked each other. Both males and females typically had higher than expected relatedness at distances <25 km, and in many distance classes greater than 25 km, less than expected relatedness. Similar patterns were apparent whether we used only loci in Hardy-Weinberg equilibrium (n = 7) or also included loci with potential null alleles (n = 5). We conclude that, contrary to expectations, sex-biased dispersal is not occurring in this species, possibly related to the reverse sexual dimorphism in this species, with females having brighter colors. We did, however, detect significant spatial genetic structure in males and females, separate and combined, showing philopatry within a genetic patch size of <25 km in C. guttata, which is concerning for an endangered species whose populations are often separated by distances greater than the genetic patch size.

Female philopatry and male-biased dispersal in a direct-developing salamander, Plethodon cinereus.

The local resource competition hypothesis and the local mate competition hypothesis were developed based on avian and mammalian systems to explain sex-biased dispersal. Most avian species show a female bias in dispersal, ostensibly due to resource defence, and most mammals show a male bias, ostensibly due to male-male competition. These findings confound phylogeny with mating strategy; little is known about sex-biased dispersal in other taxa. Resource defence and male-male competition are both intense in Plethodon cinereus, a direct-developing salamander, so we tested whether sex-biased dispersal in this amphibian is consistent with the local resource competition hypothesis (female-biased) or the local mate competition hypothesis (male-biased). Using fine-scale genetic spatial autocorrelation analyses, we found that females were philopatric, showing significant positive genetic structure in the shortest distance classes, with stronger patterns apparent when only territorial females were tested. Males showed no spatial genetic structure over the shortest distances. Mark-recapture observations of P. cinereus over 5 years were consistent with the genetic data: males dispersed farther than females during natal dispersal and 44% of females were recaptured within 1 m of their juvenile locations. We conclude that, in this population of a direct-developing amphibian, females are philopatric and dispersal is male-biased, consistent with the local mate competition hypothesis.

Multiple paternity in a salamander with socially monogamous behaviour.

In the majority of birds and mammals, social monogamy is not congruent with genetic monogamy. No research to date has compared social and genetic monogamy in amphibians. We analysed paternity in clutches of red-backed salamanders (Plethodon cinereus), a species in which social monogamy has been demonstrated in the laboratory, and 28% of individuals in the forest are found in male-female pairs in the noncourtship season. We collected 16 clutches of eggs of P. cinereus in the southern Appalachian Mountains of Virginia and collected tail clippings from attending mothers. We genotyped embryos and adults at five microsatellite loci in order to analyse paternity of clutches. Most clutches (84.6%) had multiple sires, with two to three sires per clutch. In this study, 25% of clutches had males in addition to females attending eggs. None of the mothers of these clutches were genetically monogamous. All attending males sired some of the offspring in the clutch that they attended (between 9% and 50%) but never sired a majority in that clutch. We conclude that, at least in this population, social monogamy in P. cinereus is not concomitant with genetic monogamy.