Aaron P. Wagner

Estimating relatedness and relationships using microsatellite loci with null alleles

Relatedness is often estimated from microsatellite genotypes that include null alleles. When null alleles are present, observed genotypes represent one of several possible true genotypes. If null alleles are detected, but analyses do not adjust for their presence (ie, observed genotypes are treated as true genotypes), then estimates of relatedness and relationship can be incorrect. The number of loci available in many wildlife studies is limited, and loci with null alleles are commonly a large proportion of data that cannot be discarded without substantial loss of power. To resolve this problem, we present a new approach for estimating relatedness and relationships from data sets that include null alleles. Once it is recognized that the probability of the observed genotypes is dependent on the probabilities of a limited number of possible true genotypes, the required adjustments are straightforward. The concept can be applied to any existing estimators of relatedness and relationships. We review established maximum likelihood estimators and apply the correction in that setting. In an application of the corrected method to data from striped hyenas, we demonstrate that correcting for the presence of null alleles affect results substantially. Finally, we use simulated data to confirm that this method works better than two common approaches, namely ignoring the presence of null alleles or discarding affected loci.

Symbiotic bacteria appear to mediate hyena social odors

Significance All animals are populated by microbes, and, contrary to popular belief, most microbes appear highly beneficial to their hosts. They are critical in animal nutrition and immune defense, and they can serve as important catalysts for the effective development and functioning of host tissues. It also is becoming increasingly clear that they can contribute to host behavior. It has been hypothesized that one way they do so is by producing the components of chemical signals that animals use to communicate. We tested and confirmed first predictions of this hypothesis in hyenas, demonstrating that the bacterial and odor profiles of hyena scent secretions covaried and that both profiles varied with characteristics of hyenas known to be communicated through their chemical signals. All animals harbor beneficial microbes. One way these microbes can benefit their animal hosts is by increasing the diversity and efficacy of communication signals available to the hosts. The fermentation hypothesis for mammalian chemical communication posits that bacteria in the scent glands of mammals generate odorous metabolites used by their hosts for communication and that variation in host chemical signals is a product of underlying variation in the bacterial communities inhabiting the scent glands. An effective test of this hypothesis would require accurate surveys of the bacterial communities in mammals’ scent glands and complementary data on the odorant profiles of scent secretions—both of which have been historically lacking. Here we use next-generation sequencing to survey deeply the bacterial communities in the scent glands of wild spotted and striped hyenas. We show that these communities are dominated by fermentative bacteria and that the structures of these communities covary with the volatile fatty acid profiles of scent secretions in both hyena species. The bacterial and volatile fatty acid profiles of secretions differ between spotted and striped hyenas, and both profiles vary with sex and reproductive state among spotted hyenas within a single social group. Our results strongly support the fermentation hypothesis for chemical communication, suggesting that symbiotic bacteria underlie species-specific odors in both spotted and striped hyenas and further underlie sex and reproductive state-specific odors among spotted hyenas. We anticipate that the fermentation hypothesis for chemical communication will prove broadly applicable among scent-marking mammals as others use the technical and analytical approaches used here.

Spatial grouping in behaviourally solitary striped hyaenas, Hyaena hyaena

We investigated spatial organization and patterns of interaction in a population of the little-known striped hyaena, Hyaena hyaena. We use the resulting data to test hypotheses of group formation that predict that female striped hyaenas will be solitary in response to overdispersion of food resources and males will be solitary in response to overdispersion of females. Based primarily on anecdotal or historical information, striped hyaenas have been described as solitary. We show that, as predicted, striped hyaenas of both sexes are behaviourally solitary. However, they form stable, polyandrous spatial groups composed of multiple males and a single female. We suggest that male coalition formation may be the result of male strategies to optimize trade-offs between the number of female ranges defended and the effectiveness of that defence when females are solitary and maintain large territories. Nevertheless, the joint male defence of a territory (of any size) containing only a single female would not be predicted by any major hypothesis for the evolution of group living, in this or any other species.

Evolving digital ecological networks.

“It is hard to realize that the living world as we know it is just one among many possibilities” [1]. Evolving digital ecological networks are webs of interacting, self-replicating, and evolving computer programs (i.e., digital organisms) that experience the same major ecological interactions as biological organisms (e.g., competition, predation, parasitism, and mutualism). Despite being computational, these programs evolve quickly in an open-ended way, and starting from only one or two ancestral organisms, the formation of ecological networks can be observed in real-time by tracking interactions between the constantly evolving organism phenotypes. These phenotypes may be defined by combinations of logical computations (hereafter tasks) that digital organisms perform and by expressed behaviors that have evolved. The types and outcomes of interactions between phenotypes are determined by task overlap for logic-defined phenotypes and by responses to encounters in the case of behavioral phenotypes. Biologists use these evolving networks to study active and fundamental topics within evolutionary ecology (e.g., the extent to which the architecture of multispecies networks shape coevolutionary outcomes, and the processes involved).

Patterns of relatedness and parentage in an asocial, polyandrous striped hyena population

We investigated patterns of relatedness and reproduction in a population of striped hyenas in which individuals are behaviourally solitary but form polyandrous spatial groups consisting of one adult female and multiple adult males. Group‐mate males were often close relatives, but were unrelated or distantly related in some cases, indicating that male coalitions are not strictly a result of philopatry or dispersal with cohorts of relatives. Most male–female pairs within spatial groups were unrelated or only distantly related. Considering patterns of relatedness between groups, relatedness was significantly higher among adult males living in non‐neighbouring ranges than among neighbouring males. Mean relatedness among male–female dyads was highest for group‐mates, but relatedness among non‐neighbouring males and females was also significantly higher than among dyads of opposite‐sex neighbours. Female–female relatedness also increased significantly with increasing geographic separation. These unusual and unexpected patterns may reflect selection to settle in a nonadjacent manner to reduce inbreeding and/or competition among relatives for resources (both sexes), or mates (males). Finally, resident males fathered the majority of the resident females cubs, but extra‐group paternity was likely in 31% of the cases examined, and multiple paternity was likely in half of the sampled litters.

Rabies Virus and Canine Distemper Virus in Wild and Domestic Carnivores in Northern Kenya: Are Domestic Dogs the Reservoir?

Rabies virus (RV) and canine distemper virus (CDV) can cause significant mortality in wild carnivore populations, and RV threatens human lives. We investigated serological patterns of exposure to CDV and RV in domestic dogs (Canis familiaris), African wild dogs (Lycaon pictus), black-backed jackals (Canis mesomelas), spotted hyenas (Crocuta crocuta), striped hyenas (Hyaena hyaena) and African lions (Panthera leo), over a 10-year period, in a Kenyan rangeland to assess the role domestic dogs may play in the transmission dynamics of these two important canid pathogens. Observed patterns of RV exposure suggested that repeated introduction, rather than maintenance, occurred in the wild carnivore species studied. However, RV appeared to have been maintained in domestic dogs: exposure was more likely in domestic dogs than in the wild carnivores; was detected consistently over time without variation among years; and was detected in juveniles (≤1-year-old) as well as adults (>1-year-old). We conclude that this domestic dog population could be a RV reservoir. By contrast, the absence of evidence of CDV exposure for each carnivore species examined in the study area, for specific years, suggested repeated introduction, rather than maintenance, and that CDV may require a larger reservoir population than RV. This reservoir could be a larger domestic dog population; another wildlife species; or a “metareservoir” consisting of multiple interconnected carnivore populations. Our findings suggest that RV risks to people and wild carnivores might be controlled by domestic dog vaccination, but that CDV control, if required, would need to target the species of concern.

From Cues to Signals: Evolution of Interspecific Communication via Aposematism and Mimicry in a Predator-Prey System

Current theory suggests that many signaling systems evolved from preexisting cues. In aposematic systems, prey warning signals benefit both predator and prey. When the signal is highly beneficial, a third species often evolves to mimic the toxic species, exploiting the signaling system for its own protection. We investigated the evolutionary dynamics of predator cue utilization and prey signaling in a digital predator-prey system in which prey could evolve to alter their appearance to mimic poison-free or poisonous prey. In predators, we observed rapid evolution of cue recognition (i.e. active behavioral responses) when presented with sufficiently poisonous prey. In addition, active signaling (i.e. mimicry) evolved in prey under all conditions that led to cue utilization. Thus we show that despite imperfect and dishonest signaling, given a high cost of consuming poisonous prey, complex systems of interspecific communication can evolve via predator cue recognition and prey signal manipulation. This provides evidence supporting hypotheses that cues may serve as stepping-stones in the evolution of more advanced communication and signaling systems that incorporate information about the environment.

The Roles of Standing Genetic Variation and Evolutionary History in Determining the Evolvability of Anti-Predator Strategies

Standing genetic variation and the historical environment in which that variation arises (evolutionary history) are both potentially significant determinants of a populations capacity for evolutionary response to a changing environment. Using the open-ended digital evolution software Avida, we evaluated the relative importance of these two factors in influencing evolutionary trajectories in the face of sudden environmental change. We examined how historical exposure to predation pressures, different levels of genetic variation, and combinations of the two, affected the evolvability of anti-predator strategies and competitive abilities in the presence or absence of threats from new, invasive predator populations. We show that while standing genetic variation plays some role in determining evolutionary responses, evolutionary history has the greater influence on a populations capacity to evolve anti-predator traits, i.e. traits effective against novel predators. This adaptability likely reflects the relative ease of repurposing existing, relevant genes and traits, and the broader potential value of the generation and maintenance of adaptively flexible traits in evolving populations.

Phylogenetic Comparisons Implicate Sex Hormone-Binding Globulin in “Masculinization” of the Female Spotted Hyena (Crocuta crocuta)

Exposures to sex steroids during fetal development are thought to contribute to the unique urogenital anatomy and social dominance of the female spotted hyena: overt phenotypes not shared by other hyenids (i.e. striped hyena, brown hyena, and aardwolf). Because both androgens and estrogens influence development of genitalia and behavior, and because plasma SHBG regulates their access to tissues, we compared the Shbg gene sequences, structures, and steroid-binding properties in the four extant hyenids. We found the hyenid Shbg genes (>95% identical) and mature protein sequences (98% identical) are highly conserved. As in other mammals, the hyenid SHBG all bind 5α-dihydrotestosterone with high affinity (K(d) = 0.62-1.47 nm), but they also bind estrone and dehydroepiandrosterone with similarly high affinity, and this unusual property was attributed to specific amino acids within their SHBG steroid-binding sites. Phylogenetic comparisons also indicated that the spotted hyena SHBG precursor uniquely lacks two leucine residues and has a L15W substitution within its secretion signal polypeptide, the reduced size and hydrophobicity of which markedly decreases the production of SHBG and may therefore explain why serum SHBG concentrations in male and female spotted hyenas are approximately five times lower than in other hyenids. This is important because low plasma SHBG concentrations in spotted hyenas will increase exposure to biologically active androgens and estrogen as well as to their precursors (dehydroepiandrosterone and estrone), which may contribute to the masculinized external genitalia of female spotted hyenas and to female social dominance over males.

Forces shaping major histocompatibility complex evolution in two hyena species

Abstract Genes of the mammalian major histocompatibility complex (MHC) are central to adaptive immunity. High levels of observed polymorphism at MHC loci have been hypothesized to be maintained by natural selection acting to preserve alleles for pathogen resistance. Here we examined patterns of multilocus MHC diversity in natural populations of 2 closely related carnivore species: spotted hyenas (Crocuta crocuta) and striped hyenas (Hyaena hyaena). We also tested hypotheses suggesting specific selection pressures favoring MHC diversity in these hyena species. We found several lines of evidence consistent with positive selection acting at multiple MHC loci in both species. These included high allelic variation, pervasive gene duplication, transspecies segregation of alleles, and codons evolving under positive selection that disproportionately map to known antigen-binding regions. Despite striking behavioral differences between these 2 hyaenids with respect to their mating systems and social behavior, we found no qualitative species differences in MHC loci, nor did we detect differences in the strength of natural selection. Our findings suggest that ancient shared selection pressures, including a common ancestral pattern of carrion feeding, has influenced MHC diversity more strongly in these hyena species than have selection pressures imposed relatively recently by sociality or sexual selection.