Deadbeats or losers: Discretionary male parental investment can make females less choosy.

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.

Associations between Toxoplasma gondii infection and steroid hormone levels in spotted hyenas.

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 (Crocuta crocuta, 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.

Toxoplasma gondii infections are associated with costly boldness toward felids in a wild host.

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.

Maladaptation in feral and domesticated animals.

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.

Getting Back to Nature: Feralization in Animals and Plants.

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.

Epigenetics and the maintenance of developmental plasticity: extending the signalling theory framework.

Developmental 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.

Larger females are choosier in the gray treefrog (Hyla versicolor).

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.

Surplus nest boxes and the potential for polygyny affect clutch size and offspring sex ratio in house wrens.

Females of many species can gain benefits from being choosy about their mates and even exhibit context-dependent investment in reproduction in response to the quality of their breeding situation. Here, we show that if a male house wren is provided with surplus nest boxes in his territory, his mate lays a larger clutch with a significantly higher proportion of sons. This response to a territory characteristic directly associated with male competitive ability, and ultimately to male reproductive success, suggests that male competition over access to high-quality territories with surplus nest boxes (i.e. those able to support polygyny) may influence female reproductive investment decisions. The results of this study have interesting implications, particularly considering the important role that studies of cavity nesting birds utilizing nest boxes have played in advancing our understanding of behaviour, ecology and evolution.

Context and condition dependent plasticity in sexual signaling in gray treefrogs.

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.

Signaling health versus parasites.

The Hamilton-Zuk hypothesis, that parasite-host coevolution can maintain heritable variation in fitness, has inspired a very successful research program on sexual selection on signals of health. The immunocompetence handicap hypothesis was developed to provide a handicapping mechanism to stabilize the correlation between signals and health. In earlier articles, I showed that handicap signaling is a special case, not a general law that we can rely on to deduce relative costs across signalers of different quality at equilibrium. The essential requirement for reliable signaling is that higher-quality signalers are more efficient; they get greater marginal fitness returns from an incremental increase in the signal. This does not undermine the Hamilton-Zuk hypothesis or the immunocompetence mechanism, but it does raise doubts about a widespread assumption that is commonly used to test these hypotheses: that sexual selection on signals of health implies the choice of mates with the fewest parasites. Immunity and parasites might play a fundamental role in many biological signaling systems, but viability-indicating traits are not necessarily parasite-load-indicating traits. Theory allows for the possibility that high-quality big signalers have greater health and more parasites than low-quality small signalers (and the data suggest that in many systems they do). This means that we cannot test the Hamilton-Zuk hypothesis or the immunocompetence handicap hypothesis by counting parasites. More generally, we cannot understand sexual selection on signals of health by focusing on the viability costs of signals.

Cooperative nest defence in red-winged blackbirds: reciprocal altruism, kinship or by-product mutualism?

Male red-winged blackbirds (Agelaius phoeniceus) often cooperate with their neighbours in defending nests against predators. Some studies have suggested that this is an example of by-product mutualism, whereas others have suggested the possibility of reciprocal altruism. No study has addressed the possibility of kin-selected cooperation in nest defence in this species. Reciprocal altruism, kin selection and by-product mutualism are not mutually exclusive alternatives, but few studies of territorial neighbours have tested for multiple mechanisms simultaneously. We test for these three possibilities in a population of red-winged blackbirds. We used simulated defections to test for reciprocal altruism. We used analysis of microsatellite loci to test for kin selection between adult male neighbours. We also used microsatellite loci to test for by-product mutualism resulting from nest defence of offspring sired on neighbouring territories. We found that male red-winged blackbirds cooperate in nest defence primarily as a form of reciprocal altruism. Experimental males reduced their level of nest defence relative to controls following simulated defection by a neighbour. In contrast to some earlier studies, we found no evidence for by-product mutualism: males did not defend nests where they had sired extra-pair offspring. We also found no evidence for kin selection: males were no more cooperative with more closely related neighbours. Considered alongside the results from other studies, our study suggests that mechanisms stabilizing cooperation in red-winged blackbirds may vary among populations.

Male red-winged blackbirds distrust unreliable and sexually attractive neighbours.

In many species, territorial neighbours fight to establish their mutual border and then develop a truce, known as the dear-enemy phenomenon, characterized by reduced vigilance and aggression along the border. We present evidence that among male red-winged blackbirds (Agelaius phoeniceus) the dear-enemy relationship is a form of reciprocal conditional cooperation that is stabilized, at least in part, by retaliation against cheaters. Simulated intrusions by randomly chosen neighbours were punished by a targeted increase in vigilance and aggression that persists for days. We interpret this increase in vigilance towards trespassers as a manifestation of distrust. The conditional decrease in vigilance and aggression is tempered by each neighbour's probability of cuckolding the focal male. Male red-winged blackbirds maintained greater vigilance and aggression towards sexually attractive neighbours that were more successful at extra-pair fertilizations (EPFs). It is unlikely that males directly observed neighbours copulating with their mates. They were more likely to assess a neighbour's ability to achieve extra-pair copulations using surrogate cues that correlate with success at EPFs, including body size. Our results suggest that red-winged blackbirds use rules that incorporate their neighbour's behaviour and quality in their territorial interactions with one another. Our results expand our understanding of cooperation for animals and for humans as well.

Sexually selected signals are not similar to sports handicaps.

The handicap principle is a simple but powerful metaphor that has had a major impact on how biologists study and understand sexual selection. Here, I show that its application to signalling in sexual selection is not a valid generalization from its roots in economics. Although some signalling systems, with additive costs and benefits, have solutions that resemble sports handicaps, the signalling in sexual selection has multiplicative costs and benefits, and solutions that do not resemble sports handicaps. The sports analogy is technically incorrect, metaphorically misleading and a poor guide for empirical research on the signalling in sexual selection. The evolution of sexually selected signals is not a missing piece of Darwin's puzzle; it is an integral piece of the process of evolution by natural selection, and it should be approached with the same tools that we bring to bear on the evolution of other correlated traits involved in social interactions.