Recent work indicates that feralisation is not a simple reversal of domestication, and therefore raises questions about the predictability of evolution across replicated feral populations. In the present study we compare genes and traits of two independently established feral populations of chickens (Gallus gallus) that inhabit archipelagos within the Pacific and Atlantic regions to test for evolutionary parallelism and/or divergence. We find that feral populations from each region are genetically closer to one another than other domestic breeds, despite their geographical isolation and divergent colonisation histories. Next, we used genome scans to identify genomic regions selected during feralisation (selective sweeps) in two independently feral populations from Bermuda and Hawaii. Three selective sweep regions (each identified by multiple detection methods) were shared between feral populations, and this overlap is inconsistent with a null model in which selection targets are randomly distributed throughout the genome. In the case of the Bermudian population, many of the genes present within the selective sweeps were either not annotated or of unknown function. Of the nine genes that were identifiable, five were related to behaviour, with the remaining genes involved in bone metabolism, eye development and the immune system. Our findings suggest that a subset of feralisation loci (i.e. genomic targets of recent selection in feral populations) are shared across independently established populations, raising the possibility that feralisation involves some degree of parallelism or convergence and the potential for a shared feralisation 'syndrome'.
Toxoplasma gondii is a common parasite that infects warm-blooded animals and influences host physiology. T. gondii is known to target the host's central nervous system, affecting circulating levels of steroid hormones, fear-related behaviors, and health, although these effects appear to vary among host taxa. Here, we investigated the relationship between T. gondii infection and levels of plasma testosterone and cortisol within a wild population of spotted hyenas (Crocutacrocuta, n = 109). In our analyses, we accounted for age and sex via stratified regression analyses. We detected a negative association between circulating plasma testosterone and T. gondii infection among female cubs and subadults as well as adult male hyenas. We found no associations between T. gondii infection and cortisol in any age class or sex group of hyenas. Our work adds to a growing body of literature by characterizing the relationship between T. gondii infection and physiology in a novel host in its natural habitat. In a broader context, our findings indicate that responses to infection vary with characteristics of the host and point to a clear need for additional studies and priorities for future work that include diverse taxa and ecological settings.
Recent work indicating that feralisation is not a simple reversal of domestication has raised questions about the predictability of evolutionary change across replicated feral populations. In the present study we compare genes and traits of two independently feral populations of chickens (G. gallus) inhabiting archipelagos in Pacific and Atlantic regions to test for evolutionary parallelism and/or divergence. First, we confirm purported differences in these two populations’ ancestries are corroborated by genetic and phenotypic analyses. Indeed, whereas Pacific (Kauaii) chickens recently outcrossed with wild relatives, our genetic data from Atlantic (Bermuda) chickens is more consistent with solely domestic origins encompassing diverse G. gallus breeds. Next we used genome scans to contrast the targets of feralisation (selective sweeps) between the two independently feral populations. Two sweep loci were shared between these focal populations and this overlap is inconsistent with a null model in which selection targets are randomly distributed throughout the genome. The larger set of sweep loci from the two feral genepools were also found to govern traits that were heavily modified during G. gallus’ domestication (e.g. the nervous system and behaviour, metabolism, and reproduction). Assessment of SNPs using allelic differences and SNP annotation led to candidate SNPs for further investigation for five of the genes present. Our findings suggest that a subset of feralisation loci are shared across independently-established populations, raising the possibility that feralisation involves some degree of parallelism or convergence, though a clearer understanding of possible ‘feralisation syndromes’ will require elucidating genotype-phenotype relationships in any populations being compared.
Toxoplasma gondii is hypothesized to manipulate the behavior of warm-blooded hosts to promote trophic transmission into the parasite's definitive feline hosts. A key prediction of this hypothesis is that T. gondii infections of non-feline hosts are associated with costly behavior toward T. gondii's definitive hosts; however, this effect has not been documented in any of the parasite's diverse wild hosts during naturally occurring interactions with felines. Here, three decades of field observations reveal that T. gondii-infected hyena cubs approach lions more closely than uninfected peers and have higher rates of lion mortality. We discuss these results in light of 1) the possibility that hyena boldness represents an extended phenotype of the parasite, and 2) alternative scenarios in which T. gondii has not undergone selection to manipulate behavior in host hyenas. Both cases remain plausible and have important ramifications for T. gondii's impacts on host behavior and fitness in the wild. The parasite causing toxoplasmosis can manipulate prey to behave in ways that promote transmission to the parasite's definitive feline hosts. The first study consistent with this extended phenotype in the wild finds that infected hyena cubs approach lions more closely than uninfected peers and have higher rates of lion mortality.
Males frequently compete for access to mates, sometimes at a cost to parental behaviour and self-maintenance. Theory predicts that aggressive competition among females should be less common and intense due to a trade-off between competition and future reproductive investment. However, the consequences of female aggression across the reproductive cycle are unknown in many species. In this study, we addressed four questions about female intrasexual aggression in the house wren. (1) Does intrasexual aggression help females during periods of increased competition over breeding resources? (2) Do aggressive females have higher-quality mates? (3) Do aggressive females invest less in reproduction? (4) Does female aggression affect offspring size and survival? We experimentally increased competition over nestboxes in one year by evicting a subset of birds. Females that were more aggressive during previous simulated female intrusions protected more eggs from house wren ovicide, which increased following our manipulation. In two other years, we monitored the mating patterns and reproductive performance of females. Aggressive females had mates that provided more direct benefits in the form of nestling provisioning. They did not invest less in reproduction and, in fact, provisioned their nestlings more frequently. As a result, aggressive females had heavier offspring at multiple points during development. The offspring of more aggressive females were also more likely to fledge. Overall, female aggression appeared to have fitness benefits directly following an experimental increase in competition and throughout the reproductive cycle in nonexperimental years. (C) 2019 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
There is growing interest in the alteration of host behaviors by parasites, yet crucial gaps remain in our understanding of its ecological and evolutionary significance. Here, we present the first evidence that the enhanced boldness of infected intermediate hosts of Toxoplasma gondii can increase their risk of mortality by the parasite’s definitive feline hosts. In a long-term study of hyenas in Kenya’s Masai Mara region, we found that 65% of hyenas were seropositive for T. gondii in ELISA IgG assays. Seropositive hyenas approached lions more closely than uninfected counterparts, and also showed longer latencies to approach a simulated conspecific territorial intruder. Lastly, although not significant, the ratio of mortalities caused by lions (vs. other sources) was higher for hyenas that were infected by T. gondii. These results accord with a long-standing hypothesis that the manipulation of host boldness and/or ailurophilia evolved to enhance disease transmission. Since hyenas are rarely consumed by lions, however, elevating their boldness toward lions may not be adaptive for T. gondii. Instead, it may reflect “collateral manipulation” that evolved to influence homologous mechanisms underlying behaviors of alternative hosts (e.g. rodents). This model is often invoked to explain T. gondii’s many effects in humans, but is virtually unexplored in natural settings. For T. gondii, these effects could feasibly impact both behavior and fitness in a vast array, and significant proportion, of earth’s mammals and birds. In addition to characterizing behavioral covariates of infection, we examined spatial and temporal patterns of T. gondii prevalence within the Mara landscape. Contrary to our predictions, disease prevalence did not differ 1) at a protected vs. disturbed locality, or 2) over three decades of increasing human activity within the disturbed locality.
Toxoplasma gondii is widely reported to manipulate the behavior of its non-definitive hosts in ways that promote lethal interactions with the parasite’s definitive feline hosts. Nonetheless, there is a lack of data on the association between T. gondii infection and costly behavioral interactions with felids in nature. Here, we report that three decades of field observations reveal T. gondii infected hyena cubs approach lions more closely than uninfected peers and have higher rates of lion mortality. Our findings support the hypothesis that T. gondii’s manipulation of host boldness is an extended phenotype that promotes parasite transmission from intermediate hosts to feline predators. While upregulating hyena boldness toward lions might achieve this, it may also reflect a collateral influence of manipulative traits that evolved in other hosts (e.g., rodents). In either case, our findings corroborate the potential impacts of a globally distributed and generalist parasite ( T. gondii ) on fitness-related interaction with felids in a wild host. One Sentence Summary Wild hyenas infected with the parasite T. gondii show evidence of costly behavioral manipulation when interacting with lions.
Selection regimes and population structures can be powerfully changed by domestication and feralization, and these changes can modulate animal fitness in both captive and natural environments. In this review, we synthesize recent studies of these two processes and consider their impacts on organismal and population fitness. Domestication and feralization offer multiple windows into the forms and mechanisms of maladaptation. Firstly, domestic and feral organisms that exhibit suboptimal traits or fitness allow us to identify their underlying causes within tractable research systems. This has facilitated significant progress in our general understandings of genotype-phenotype relationships, fitness trade-offs, and the roles of population structure and artificial selection in shaping domestic and formerly domestic organisms. Additionally, feralization of artificially selected gene variants and organisms can reveal or produce maladaptation in other inhabitants of an invaded biotic community. In these instances, feral animals often show similar fitness advantages to other invasive species, but they are also unique in their capacities to modify natural ecosystems through introductions of artificially selected traits. We conclude with a brief consideration of how emerging technologies such as genome editing could change the tempos, trajectories, and ecological consequences of both domestication and feralization. In addition to providing basic evolutionary insights, our growing understanding of mechanisms through which artificial selection can modulate fitness has diverse and important applications-from enhancing the welfare, sustainability, and efficiency of agroindustry, to mitigating biotic invasions.
Formerly domesticated organisms and artificially selected genes often escape controlled cultivation, but their subsequent evolution is not well studied. In this review, we examine plant and animal feralization through an evolutionary lens, including how natural selection, artificial selection, and gene flow shape feral genomes, traits, and fitness. Available evidence shows that feralization is not a mere reversal of domestication. Instead, it is shaped by the varied and complex histories of feral populations, and by novel selection pressures. To stimulate further insight we outline several future directions. These include testing how 'domestication genes' act in wild settings, studying the brains and behaviors of feral animals, and comparative analyses of feral populations and taxa. This work offers feasible and exciting research opportunities with both theoretical and practical applications.
Individuals should fight hardest when they stand to lose the most. Whereas males frequently compete for fertile females, females more often compete for high quality males, male care, or resources required to breed. We asked whether established, territorial female house wrens (Troglodytes aedon) challenged by simulated female intruders fight as if they place more value on retaining (1) their nesting cavity or (2) exclusive access to other benefits offered by males. We randomly assigned house wren pairs to receive one or three nest boxes and then assayed female aggression. The relative costs to losing differed between box treatments. For one-box females, the risk of losing the cavity and territory was higher. For three-box females, the risk of losing the cavity may be lower because intruders may be able to settle as secondary females in the supplemental boxes. In this situation, females would lose exclusive access to males and their territories but would still retain the male's assistance rearing offspring since male house wrens favour their oldest brood. We found that one-box females were significantly more aggressive. This response may be adaptive, as females that switched territories between broods were significantly more likely to lose their entire nest prior to hatching than females that retained the same territory. We interpret our results to mean that female house wrens value the nest cavity more than other benefits from exclusive access to males and their territories. This work contributes to a body of evidence that females often compete for resources required to breed.
We present a mathematical model of aggressive mimicry systems in which predators lure prey by mimicking food items of those prey. We use this model to explore potential dynamics of mimicry systems where a bad outcome results in death. This leads to some counterintuitive expectations not found in earlier models of aggressive mimicry that have not included the potential for dupe death. Abstract Aggressive mimicry is a widespread phenomenon in which predators use resemblance to objects in the environment to exploit organisms that make discrimination errors (dupes). Aggressive mimics harm dupes in several ways, including predation, parasitism (including brood parasitism), and infection. Previous models of aggressive mimicry have been built from models originally derived for protective mimicries where the risk of death to dupes was not considered. Some kinds of aggressive mimicry carry significant risk of death for the dupes. Death changes things in significant ways that may be better modeled using the techniques developed for understanding foraging under predation risk. We present a simple model of a common type of aggressive mimicry system in which mimics are predators and lure dupes by mimicry of a food resource. The model combines a simple model for foraging under risk of predation with signal detection theory. This modeling approach reveals 2 contrasting potential responses of dupes to mimics. Counterintuitively, dupes might be selected to become either more or less discriminating and risk averse as predators become more common or more memetic, depending on starting conditions relating to alternative resources available to the dupes. Implications of these divergent trajectories for aggressive mimicry systems are explored.
ABSTRACTDevelopmental plasticity, a phenomenon of importance in both evolutionary biology and human studies of the developmental origins of health and disease (DOHaD), enables organisms to respond to their environment based on previous experience without changes to the underlying nucleotide sequence. Although such phenotypic responses should theoretically improve an organism's fitness and performance in its future environment, this is not always the case. Herein, we first discuss epigenetics as an adaptive mechanism of developmental plasticity and use signaling theory to provide an evolutionary context for DOHaD phenomena within a generation. Next, we utilize signalling theory to identify determinants of adaptive developmental plasticity, detect sources of random variability – also known as process errors that affect maintenance of an epigenetic signal (DNA methylation) over time, and discuss implications of these errors for an organism's health and fitness. Finally, we apply life‐course epidemiology conceptual models to inform study design and analytical strategies that are capable of parsing out the potential effects of process errors in the relationships among an organism's early environment, DNA methylation, and phenotype in a future environment. Ultimately, we hope to foster cross‐talk and interdisciplinary collaboration between evolutionary biology and DOHaD epidemiology, which have historically remained separate despite a shared interest in developmental plasticity.
Two of the most important reproductive decisions that animals face are how to choose mates and how to invest in offspring. In species where both males and females provide offspring care, these selection pressures will often be reciprocally intertwined: mate preferences may depend on parental investment patterns while parental investment patterns may depend on mate preferences. We describe and analyze a mathematical model of this interaction, in which females can choose amongst males who have high attractiveness or low attractiveness, while males can decide whether to provide offspring care. We compare the case where males decide whether to provide care to the cases where males always provide care and where they never provide care. For a wide range of parameter settings, we find that when males decide whether to provide care, females are selected to be less choosy. This reduction in female choosiness occurs even though discretionary male care leads to greater variation among males in their offspring output. This finding contrasts with previous theoretical studies, and is driven by our assumption that males can decide whether to help provide care after mating occurs. Our results show how the interdependencies between mate choice and parental care can generate outcomes that can only be understood by considering both processes simultaneously.
For many species sexual signaling is a very costly activity, both in terms of energetic expenditure and increased conspicuousness to predators. One potential strategy to limit the costs of signaling is to only signal at maximum effort in contexts when signaling is expected to be most effective. Multiple studies have documented extensive plasticity in sexual signaling within a variety of contexts, however fewer experiments have examined individual-level variation in the extent of signaling plasticity and the causes of this variation. In this study we examined the influence of size and physical condition on the magnitude of signaling plasticity using a gray treefrog (Hyla versicolor) study system. We quantified signaling plasticity by recording male calling behavior first in the absence and then in the presence of a sexually receptive female. For one call property, call length, we found that both weight and condition had a significant influence on the magnitude of plasticity. Smaller males, and males in higher condition exhibited the greatest degree of plasticity. We discuss several possible explanations for this pattern and provide suggestions for future work to examine the consequences of this plasticity and the potential interactive effects of multiple biotic and abiotic contexts on signaling plasticity.
Current models indicate that an organism’s sensitivity to risk may be heavily influenced by the trade-off between current and future reproduction. Individuals that have fewer future reproductive opportunities are expected to show more risky behavior as they have less to lose if captured by a predator (the asset protection principle). In this study, we examined the effects of age and physical condition on risk taking behavior during sexual signaling in the gray treefrog (Hyla versicolor) to test the prediction that older and poor condition males will take greater risks than their younger or higher-condition counterparts. In accordance with these predictions, we found that males in low physical condition resumed signaling activity more rapidly following a simulated predator attack than their higher-condition counterparts, although this effect was only apparent in one of two study years. Further, males that resumed calling early did not offset their risk of detection by predators via reduced calling effort. Contrary to our predictions, we did not find age to be a significant predictor of risk taking in male signaling behavior. We conclude with a discussion of possible explanations for the discrepancy observed between years and highlight the potential reproductive consequences of variation in risk taking behavior.
Individual variation in female mate choice has important implications for sexual trait evolution and the maintenance of phenotypic diversity. In this study we examined several potential drivers of individual variation in female choosiness for the well-studied, energetically expensive courtship signal of male gray treefrogs, Hyla versicolor. Specifically, we investigated the relationship between female choosiness and other female traits (female body size, physical condition, and age) using a costly choice playback experiment where females traveled different simulated distances to reach attractive mates. We found that larger females maintained their preferences for attractive male calls over greater simulated distances (i.e. were choosier) than smaller females. We discuss possible explanations for why larger females may be choosier and suggest several potential avenues of future research.
Birdsong in temperate zone passerines is a trait under sexual selection in males. Female song is still thought to be rare in this group. Here we show that female song is common in a temperate zone population of house wrens, Troglodytes aedon, and we provide evidence for its functional role in defending against male and female conspecifics. We observed that females sang most frequently at the onset of egg laying, with song becoming less common as incubation approached. Thus, females sang most during the time when eggs were left unguarded and susceptible to conspecific attack. We also conducted playback experiments to test whether conspecific stimuli would induce female song in focal individuals. Playback from both male and female conspecifics elicited strong song responses from resident females, who often vocalized independently from their partners. However, females were more physically aggressive towards female songs than male songs. Finally, females that sang more during these simulated conspecific intrusions ultimately lost fewer eggs to house wren ovicide. These results suggest that female house wren song may have evolved, at least in part, for use in intra-and intersexual competition. These results also highlight how investigating these traditionally male behaviours in female animals can lead to key insights regarding the evolution of sexual dimorphism. (C) 2016 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.