Ryan R. Germain

Quantifying inbreeding avoidance through extra-pair reproduction

Extra‐pair reproduction is widely hypothesized to allow females to avoid inbreeding with related socially paired males. Consequently, numerous field studies have tested the key predictions that extra‐pair offspring are less inbred than females’ alternative within‐pair offspring, and that the probability of extra‐pair reproduction increases with a females relatedness to her socially paired male. However, such studies rarely measure inbreeding or relatedness sufficiently precisely to detect subtle effects, or consider biases stemming from failure to observe inbred offspring that die during early development. Analyses of multigenerational song sparrow (Melospiza melodia) pedigree data showed that most females had opportunity to increase or decrease the coefficient of inbreeding of their offspring through extra‐pair reproduction with neighboring males. In practice, observed extra‐pair offspring had lower inbreeding coefficients than females’ within‐pair offspring on average, while the probability of extra‐pair reproduction increased substantially with the coefficient of kinship between a female and her socially paired male. However, simulations showed that such effects could simply reflect bias stemming from inbreeding depression in early offspring survival. The null hypothesis that extra‐pair reproduction is random with respect to kinship therefore cannot be definitively rejected in song sparrows, and existing general evidence that females avoid inbreeding through extra‐pair reproduction requires reevaluation given such biases.

Color expression in experimentally regrown feathers of an overwintering migratory bird: implications for signaling and seasonal interactions

Plumage coloration in birds plays a critical role in communication and can be under selection throughout the annual cycle as a sexual and social signal. However, for migratory birds, little is known about the acquisition and maintenance of colorful plumage during the nonbreeding period. Winter habitat could influence the quality of colorful plumage, ultimately carrying over to influence sexual selection and social interactions during the breeding period. In addition to the annual growth of colorful feathers, feather loss from agonistic interactions or predator avoidance could require birds to replace colorful feathers in winter or experience plumage degradation. We hypothesized that conditions on the wintering grounds of migratory birds influence the quality of colorful plumage. We predicted that the quality of American redstart (Setophaga ruticilla) tail feathers regrown after experimental removal in Jamaica, West Indies, would be positively associated with habitat quality, body condition, and testosterone. Both yearling (SY) and adult (ASY) males regrew feathers with lower red chroma, suggesting reduced carotenoid content. While we did not observe a change in hue in ASY males, SY males shifted from yellow to orange plumage resembling experimentally regrown ASY feathers. We did not observe any effects of habitat, testosterone, or mass change. Our results demonstrate that redstarts are limited in their ability to adequately replace colorful plumage, regardless of habitat, in winter. Thus, feather loss on the nonbreeding grounds can affect social signals, potentially negatively carrying over to the breeding period.

Using multi-scale distribution and movement effects along a montane highway to identify optimal crossing locations for a large-bodied mammal community

Roads are a major cause of habitat fragmentation that can negatively affect many mammal populations. Mitigation measures such as crossing structures are a proposed method to reduce the negative effects of roads on wildlife, but the best methods for determining where such structures should be implemented, and how their effects might differ between species in mammal communities is largely unknown. We investigated the effects of a major highway through south-eastern British Columbia, Canada on several mammal species to determine how the highway may act as a barrier to animal movement, and how species may differ in their crossing-area preferences. We collected track data of eight mammal species across two winters, along both the highway and pre-marked transects, and used a multi-scale modeling approach to determine the scale at which habitat characteristics best predicted preferred crossing sites for each species. We found evidence for a severe barrier effect on all investigated species. Freely-available remotely-sensed habitat landscape data were better than more costly, manually-digitized microhabitat maps in supporting models that identified preferred crossing sites; however, models using both types of data were better yet. Further, in 6 of 8 cases models which incorporated multiple spatial scales were better at predicting preferred crossing sites than models utilizing any single scale. While each species differed in terms of the landscape variables associated with preferred/avoided crossing sites, we used a multi-model inference approach to identify locations along the highway where crossing structures may benefit all of the species considered. By specifically incorporating both highway and off-highway data and predictions we were able to show that landscape context plays an important role for maximizing mitigation measurement efficiency. Our results further highlight the need for mitigation measures along major highways to improve connectivity between mammal populations, and illustrate how multi-scale data can be used to identify preferred crossing sites for different species within a mammal community.

Phenotypic divergence during speciation is inversely associated with differences in seasonal migration.

Differences in seasonal migration might promote reproductive isolation and differentiation by causing populations in migratory divides to arrive on the breeding grounds at different times and/or produce hybrids that take inferior migratory routes. We examined this question by quantifying divergence in song, colour, and morphology between sister pairs of North American migratory birds. We predicted that apparent rates of phenotypic differentiation would differ between pairs that do and do not form migratory divides. Consistent with this prediction, results from mixed effects models and Ornstein–Uhlenbeck models of evolution showed different rates of divergence between these groups; surprisingly, differentiation was greater among non-divide pairs. We interpret this finding as a result of variable rates of population blending and fusion between partially diverged forms. Ancient pairs of populations that subsequently fused are now observed as a single form, whereas those that did not fuse are observable as pairs and included in our study. We propose that fusion of two populations is more likely to occur when they have similar migratory routes and little other phenotypic differentiation that would cause reproductive isolation. By contrast, pairs with migratory divides are more likely to remain reproductively isolated, even when differing little in other phenotypic traits. These findings suggest that migratory differences may be one among several isolating barriers that prevent divergent populations from fusing and thereby increase the likelihood that they will continue differentiating as distinct species.

Delayed maturation of multiple signals in a migratory songbird

Many animals use multiple signals in sexual communication, but our understanding of the interactions between multiple signals, particularly in inexperienced breeders, is limited. In birds, delayed plumage maturation (DPM) is well documented; young birds appear duller than adults, despite reaching sexual maturity. Age-related changes in song structure are also common in songbirds, though the extent to which songs of yearling males differ from those of adults (delayed song maturation, DSM) and its prevalence in species with DPM is unknown. We tested for DSM in the mate-attraction (repeat) song of a species with dramatic DPM, the American redstart (Setophaga ruticilla). Repeat song structure of territorial yearling and adult males differed significantly, based on discriminant analysis of nine non-collinear song features. Combined with previous evidence of delayed maturation in territorial (serial) song, we provide the first evidence for DSM in different song types used in different behavioral contexts during the breeding season of a migratory songbird. Within adults, variation in repeat song was associated with pairing, earlier onset of breeding, and number of offspring sired, suggesting a potential benefit for expressing more adult-like song. We found no relationship between the expression of adult-like repeat song and plumage in either age class. These results indicate that delayed maturation of repeat song in yearling redstarts is not due to a generalized delay in signal development, and suggest further work is needed to determine whether mate attraction (for both yearling and adult males) provides greater pressure to sound more “adult-like” than to look more “adult-like”.

The Consequences of Polyandry for Sibship Structures, Distributions of Relationships and Relatedness, and Potential for Inbreeding in a Wild Population

The evolutionary benefits of simultaneous polyandry (female multiple mating within a single reproductive event) remain elusive. One potential benefit could arise if polyandry alters sibship structures and consequent relationships and relatedness among females’ descendants, thereby intrinsically reducing future inbreeding risk (the indirect inbreeding avoidance hypothesis). However such effects have not been quantified in naturally complex mating systems that also encompass iteroparity, overlapping generations, sequential polyandry, and polygyny. We used long-term social and genetic pedigree data from song sparrows (Melospiza melodia) to quantify cross-generational consequences of simultaneous polyandry for offspring sibship structures and distributions of relationships and relatedness among possible mates. Simultaneous polyandry decreased full sibships and increased half-sibships, on average, but such effects varied among females and were smaller than would occur in the absence of sequential polyandry or polygyny. Further, while simultaneous polyandry decreased the overall frequencies of possible matings among adult full sibs, it increased the frequencies of possible matings among adult half-sibs and more distant relatives. These results imply that the intrinsic consequences of simultaneous polyandry for inbreeding risk could cause weak indirect selection on polyandry, but the magnitude and direction of such effects will depend on complex interactions with other mating system components and the form of inbreeding depression.

Evolution of precopulatory and post-copulatory strategies of inbreeding avoidance and associated polyandry

Inbreeding depression is widely hypothesized to drive adaptive evolution of precopulatory and post‐copulatory mechanisms of inbreeding avoidance, which in turn are hypothesized to affect evolution of polyandry (i.e. female multiple mating). However, surprisingly little theory or modelling critically examines selection for precopulatory or post‐copulatory inbreeding avoidance, or both strategies, given evolutionary constraints and direct costs, or examines how evolution of inbreeding avoidance strategies might feed back to affect evolution of polyandry. Selection for post‐copulatory inbreeding avoidance, but not for precopulatory inbreeding avoidance, requires polyandry, whereas interactions between precopulatory and post‐copulatory inbreeding avoidance might cause functional redundancy (i.e. ‘degeneracy’) potentially generating complex evolutionary dynamics among inbreeding strategies and polyandry. We used individual‐based modelling to quantify evolution of interacting precopulatory and post‐copulatory inbreeding avoidance and associated polyandry given strong inbreeding depression and different evolutionary constraints and direct costs. We found that evolution of post‐copulatory inbreeding avoidance increased selection for initially rare polyandry and that evolution of a costly inbreeding avoidance strategy became negligible over time given a lower‐cost alternative strategy. Further, fixed precopulatory inbreeding avoidance often completely precluded evolution of polyandry and hence post‐copulatory inbreeding avoidance, but fixed post‐copulatory inbreeding avoidance did not preclude evolution of precopulatory inbreeding avoidance. Evolution of inbreeding avoidance phenotypes and associated polyandry is therefore affected by evolutionary feedbacks and degeneracy. All else being equal, evolution of precopulatory inbreeding avoidance and resulting low polyandry is more likely when post‐copulatory inbreeding avoidance is precluded or costly, and evolution of post‐copulatory inbreeding avoidance greatly facilitates evolution of costly polyandry.

Examination of context-dependent effects of natal traits on lifetime reproductive success using a long-term study of a temperate songbird

ABSTRACT Identifying the causes of individual variation in fitness should improve predictions about population dynamics and responses of populations to environmental change. Precise predictions may require long-term studies to parameterize models when the fitness of individual phenotypes depends on environmental conditions. We used a 37-yr study of a resident Song Sparrow (Melospiza melodia) population to identify traits that predicted individual variation in female lifetime reproductive success and to test for context dependence in trait–fitness relationships. Specifically, we asked how individual inbreeding coefficient, maternal age, and a suite of natal morphological traits influenced 2 components of lifetime reproductive success: (1) the probability of surviving to breed, and (2) the lifetime number of offspring produced, given that a female bred locally. We then tested whether population density influenced trait–fitness relationships. We found that differences in natal traits had life-long impacts on female fitness. Lower maternal age, a higher inbreeding coefficient, later laying date, lower nestling body condition, and longer tarsi were all negatively related to lifetime reproductive success. Maternal age and the inbreeding coefficient influenced both components of lifetime reproductive success, whereas other factors only influenced one. Therefore, traits that predict the probability of surviving to breed locally may differ from those that predict the number of offspring produced. We also observed larger effects of the inbreeding coefficient on fitness in years of low population density, which were often preceded by cool winters. Our findings demonstrate that natal traits and the environment experienced early in a birds life can have life-long effects on individual fitness, primarily independent of population density.

Demographic consequences of invasion by a native, controphic competitor to an insular bird population

Species invasions and range shifts can lead to novel competitive interactions between historically resident and colonizing species, but the demographic consequences of such interactions remain controversial. We present results from field experiments and 45 years of demographic monitoring to test the hypothesis that the colonization of Mandarte Is., BC, Canada, by fox sparrows (Passerella iliaca) caused the long-term decline of the resident population of song sparrows (Melospiza melodia). Several lines of evidence indicate that competition with fox sparrows for winter food reduced over-winter survival in juvenile song sparrows by 48% from 1960 to 2015, enforcing population decline despite an increase in annual reproductive rate in song sparrows over the same period. Preference for locally abundant seeds presented at experimental arenas suggested complete overlap in diet in song and fox sparrows, and observations at arenas baited with commercial seed showed that fox sparrows displaced song sparrows in 91–100% of interactions in two periods during winter. In contrast, we found no evidence of interspecific competition for resources during the breeding season. Our results indicate that in the absence of marked shifts in niche dimension, range expansions by dominant competitors have the potential to cause the extirpation of historically resident species when competitive interactions between them are strong and resources not equitably partitioned.

No evidence of inbreeding depression in sperm performance traits in wild song sparrows

Abstract Inbreeding is widely hypothesized to shape mating systems and population persistence, but such effects will depend on which traits show inbreeding depression. Population and evolutionary consequences could be substantial if inbreeding decreases sperm performance and hence decreases male fertilization success and female fertility. However, the magnitude of inbreeding depression in sperm performance traits has rarely been estimated in wild populations experiencing natural variation in inbreeding. Further, the hypothesis that inbreeding could increase within‐ejaculate variation in sperm traits and thereby further affect male fertilization success has not been explicitly tested. We used a wild pedigreed song sparrow (Melospiza melodia) population, where frequent extrapair copulations likely create strong postcopulatory competition for fertilization success, to quantify effects of male coefficient of inbreeding (f) on key sperm performance traits. We found no evidence of inbreeding depression in sperm motility, longevity, or velocity, and the within‐ejaculate variance in sperm velocity did not increase with male f. Contrary to inferences from highly inbred captive and experimental populations, our results imply that moderate inbreeding will not necessarily constrain sperm performance in wild populations. Consequently, the widely observed individual‐level and population‐level inbreeding depression in male and female fitness may not stem from reduced sperm performance in inbred males.