Eric B. Liebgold

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.

Dispersal Versus Site Tenacity of Adult and Juvenile Red-Backed Salamanders (Plethodon cinereus)

Abstract In many species of amphibians that display territoriality, it is unclear at what life stage and to what extent dispersal occurs. We examined whether differences existed between life stages in dispersal and homing in red-backed salamanders (Plethodon cinereus) in continuous habitat. In a mark–recapture study, we found that juvenile and adult movements between years were not significantly different. The median distances moved by both adults (0.85–0.88 m) and juveniles (1.14–1.22 m) of P. cinereus between years were similar to the diameter of adult home ranges in this area (1.15 m). In a homing experiment, we found that, although the probability of recapture of translocated individuals under their original cover object increased with body size, both adults and juveniles successfully orientated toward their original cover objects when displaced over short distances (1.5 m and 6.25 m), but their orientation was random when displaced long distances (12.5 m and 25 m). Despite the current assumption that juveniles of P. cinereus lack territorial behaviors, our results suggest that regardless of life stage, site tenacity accounts for lack of movements.

JUVENILE MOVEMENTS AND POTENTIAL INTER-AGE CLASS ASSOCIATIONS OF RED-BACKED SALAMANDERS

For many taxa, little is known about whether territoriality of adults affects the behavior of juveniles. Laboratory research has shown that aggression of adult territorial red-backed salamanders (Plethodon cinereus) decreases with familiarity, but it is not clear whether juveniles are randomly or nonrandomly associated with adult or parental territories. Using data from mark-recapture surveys, we compared the number of captures of first-year juveniles and adults of P. cinereus to ambient meteorological data. We found no evidence for temporal separation of foraging; weather conditions did not affect the proportion of first-year juveniles captured. We then conducted nearest-neighbor analyses to evaluate whether first-year juveniles were spatially associated with or disassociated from adult home ranges. Juveniles were neither closer to nor further away from adults than would be expected by random chance. Nearest-neighbor distances also were not significantly different from the mean radius of adult home ranges. There was no evidence that the distribution of adult home ranges affected the distribution of juveniles, at least after recent rainfall events; there is a possibility that interactions between age classes may occur under drier conditions.

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 mark–recapture 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.

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.

Differential Survival and the Effects of Predation on a Color Polymorphic Species, the Red-Backed Salamander (Plethodon cinereus)

Abstract Color polymorphism is common in many species, and color morph frequency is affected by differences in ecological and evolutionary pressures on each color morph. Plethodon cinereus, the Red-Backed Salamander, has two common color morphs, striped and unstriped, that vary in frequency among populations. Plethodon cinereus color morphs differ in their escape behaviors when exposed to predators and in their tail autotomization rates; this may result from differential predation. Although these previous studies indirectly implicated differential predation, we directly tested the hypothesis that color morphs differed in survival and whether one morph was depredated at a higher rate. We determined the survival of each color morph over 3 yr with the use of mark–recapture data. We first compared frequencies of color morphs in juveniles and adults, and then estimated whether color morphs had different survival rates with the statistical program MARK. We found that frequency of striped salamanders was lower in adults than in juveniles, implying that fewer striped individuals survived to adulthood. In addition, color and age best explained survival probability during spring, but not fall, seasons. To test the effects of color morph on predation experimentally, we used clay models to determine the effects of avian and mammalian predators. We found more attacks on striped clay models by avian predators compared to the unstriped models, but we found no difference in attacks by mammals. Overall, these results support the hypothesis that there is differential predation in P. cinereus, with more predation on, and lower survival in, the striped morph.

Heterozygosity–behavior and heterozygosity–fitness correlations in a salamander with limited dispersal

Inbreeding and genetic drift can decrease genetic heterozygosity, and this low heterozygosity can depress fitness, resulting in heterozygosity–fitness correlations (HFCs). HFCs are typically small in magnitude, a result often attributed to power of the analyses. Animal behaviors often affect fitness and are often heritable to some degree. We hypothesized that heterozygosity influences behavior, which, in turn, potentially influences fitness. Specifically, in red-backed salamanders, Plethodon cinereus, which have limited dispersal and the potential for inbreeding, we tested whether heterozygosity, as estimated from six microsatellite loci, affected home range size, juvenile growth, and survival. We found that salamanders with higher heterozygosity had larger home ranges and grew faster, which is indicative of reproductive success. However, we found no effects of heterozygosity on survival. We conclude that, because activity in P. cinereus is tightly linked to food uptake and mass gain, heterozygosity influences growth via effects on foraging behavior. Future research should investigate how the relationship between heterozygosity, behavior, and fitness may be affected or mediated by endocrine or immune systems.