Genetic diversity of honeybee colonies predicts gut bacterial diversity of individual colony members.

The gut microbiota of social bees is relatively simple and dominated by a set of core taxa found consistently in individuals around the world. Yet, variation remains and can affect host health. We characterized individual- and regional-scale variation in honeybee (Apis mellifera) gut microbiota from 64 colonies in North-West England by sequencing the V4 region of the 16S rRNA gene and asked whether microbiota were influenced by host genotype and landscape composition. We also characterized the genotypes of individual bees and the land cover surrounding each colony. The literature-defined core taxa dominated across the region despite the varied environments. However, there was variation in the relative abundance of core taxa, and colony membership explained much of this variation. Individuals from more genetically diverse colonies had more diverse microbiotas, but individual genetic diversity did not influence gut microbial diversity. There were weak trends for colonies in more similar landscapes to have more similar microbiota, and for bees from more urban landscapes to have less diverse microbiota. To our knowledge, this is the first report for any species that the gut bacterial communities of individuals are influenced by the genotypes of others in the population.

Like Father Like Son: Cultural and Genetic Contributions to Song Inheritance in an Estrildid Finch.

Social learning of vocalizations is integral to song inheritance in oscine passerines. However, other factors, such as genetic inheritance and the developmental environment, can also influence song phenotype. The relative contributions of these factors can have a strong influence on song evolution and may affect important evolutionary processes such as speciation. However, relative contributions are well-described only for a few species and are likely to vary with taxonomy. Using archived song data, we examined patterns of song inheritance in a domestic population of Java sparrows (Lonchura oryzivora), some of which had been cross-fostered. Six-hundred and seventy-six songs from 73 birds were segmented and classified into notes and note subtypes (N = 22,972), for which a range of acoustic features were measured. Overall, we found strong evidence for cultural inheritance of song structure and of the acoustic characteristics of notes; sons' song syntax and note composition were similar to that of their social fathers and were not influenced by genetic relatedness. For vocal consistency of note subtypes, a measure of vocal performance, there was no apparent evidence of social or genetic inheritance, but both age and developmental environment influenced consistency. These findings suggest that high learning fidelity of song material, i.e., song structure and note characteristics, could allow novel variants to be preserved and accumulate over generations, with implications for evolution and conservation. However, differences in vocal performance do not show strong links to cultural inheritance, instead potentially serving as condition dependent signals.

The uses and implications of avian vocalizations for conservation planning.

There is a growing recognition that animal behavior can affect wildlife conservation, but there have been few direct studies of animal behavior in conservation programs. However, a great deal of existing behavioral research can be applied in the context of conservation. Research on avian vocalizations provides an excellent example. The conspicuous nature of the vocal behavior of birds makes it a useful tool for monitoring populations and measuring biodiversity, but the importance of vocalizations in conservation goes beyond monitoring. Geographic song variants with population-specific signatures, or dialects, can affect territory formation and mate choice. Dialects are influenced by cultural evolution and natural selection and changes can accumulate even during the timescale of conservation interventions, such as translocations, reintroductions, and ex situ breeding. Information from existing research into avian vocalizations can be used to improve conservation planning and increase the success of interventions. Vocalizations can confer a number of benefits for conservation practitioners through monitoring, providing baseline data on populations and individuals. However, the influence of cultural variation on territory formation, mate choice, and gene flow should be taken into account because cultural differences could create obstacles for conservation programs that bring birds from multiple populations together and so reduce the success of interventions.

Implicaciones y Usos de las Vocalizaciones de Aves para la Conservación de la Planeación Resumen Hay un creciente reconocimiento de que el comportamiento animal puede afectar a la conservación de la fauna, pero ha habido pocos estudios directos del comportamiento animal en los programas de conservación. Sin embargo, una gran cantidad de la investigación existente sobre el comportamiento puede aplicarse en el contexto de la conservación. Las investigaciones sobre las vocalizaciones de aves son un excelente ejemplo. La naturaleza conspicua del comportamiento vocal de las aves hace que sea una herramienta útil para el monitoreo de las poblaciones y las medidas de la biodiversidad, pero la importancia de las vocalizaciones en la conservación va más allá del monitoreo. Las variantes geográficas de canto con firmas específicas para cada población, también conocidas como dialectos, pueden afectar a la formación del territorio y a la elección de pareja. Los dialectos están influenciados por la evolución cultural y la selección natural y los cambios pueden acumularse incluso durante la escala de tiempo de las intervenciones de conservación, como las reubicaciones, las reintroducciones y la reproducción ex situ. La información disponible a partir de las investigaciones existentes sobre las vocalizaciones de aves puede usarse para mejorar la planeación de la conservación e incrementar el éxito de las intervenciones. Las vocalizaciones pueden otorgar un número de beneficios para quienes practican la conservación a través del monitoreo, proporcionando información de la línea base de las poblaciones y los individuos. Sin embargo, la influencia de la variación cultural sobre la formación del territorio, la elección de pareja y el flujo génico deberían considerarse ya que las diferencias culturales podrían crear obstáculos para los programas de conservación que agrupan a aves de diferentes poblaciones y con ello reducen el éxito de las intervenciones.

Competition for resources can promote the divergence of social learning phenotypes.

Social learning occurs when animals acquire knowledge or skills by observing or interacting with others and is the fundamental building block of culture. Within populations, some individuals use social learning more frequently than others, but why social learning phenotypes differ among individuals is poorly understood. We modelled the evolution of social learning frequency in a system where foragers compete for resources, and there are many different foraging options to learn about. Social learning phenotypes diverged when some options offered much better rewards than others and expected rewards changed moderately quickly over time. When options offered similar rewards or when rewards changed slowly, a single social learning phenotype evolved. This held for fixed and simple conditional social learning rules. Sufficiently complex conditional social learning rules prevented the divergence of social learning phenotypes under all conditions. Our results explain how competition can promote the divergence of social learning phenotypes.

Left-handedness is associated with greater fighting success in humans.

Left-handedness is a costly, sexually dimorphic trait found at low frequencies in all human populations. How the handedness polymorphism is maintained is unclear. The fighting hypothesis argues that left-handed men have a negative frequency-dependent advantage in violent intrasexual competition giving them a selective advantage. In support of this, many studies have found that left-handed men are overrepresented among modern professional fighters, but studies typically find no difference in fighting success between left and right-handed fighters. We studied over 13,800 professional boxers and mixed martial artists of varying abilities in three of the largest samples to test this hypothesis to date, finding robust evidence that left-handed fighters have greater fighting success. This held for both male and female fighters, and for both percentage of fights won and an objective measure of fighting ability. We replicated previous results showing that left-handed fighters are strongly overrepresented in professional combat sports, but left-handed fighters did not show greater variance in fighting ability, a hypothesis suggested in previous studies. Overall we find strong evidence consistent with the fighting hypothesis.

Reproductive skew affects social information use.

Individuals vary in their propensity to use social learning, the engine of cultural evolution, to acquire information about their environment. The causes of those differences, however, remain largely unclear. Using an agent-based model, we tested the hypothesis that as a result of reproductive skew differences in energetic requirements for reproduction affect the value of social information. We found that social learning is associated with lower variance in yield and is more likely to evolve in risk-averse low-skew populations than in high-skew populations. Reproductive skew may also result in sex differences in social information use, as empirical data suggest that females are often more risk-averse than males. To explore how risk may affect sex differences in learning strategies, we simulated learning in sexually reproducing populations where one sex experiences more reproductive skew than the other. When both sexes compete for the same resources, they tend to adopt extreme strategies: the sex with greater reproductive skew approaches pure individual learning and the other approaches pure social learning. These results provide insight into the conditions that promote individual and species level variation in social learning and so may affect cultural evolution.

Targeted metagenomics approach to capture the biodiversity of Saccharomyces genus in wild environments.

The species of the genus Saccharomyces are commonly inhabiting tree bark and the surrounding soil, but their abundance have likely been underestimated due to biases in culturing methods. Metagenomic studies have so far been unable to detect Saccharomyces species in wild environments. Here, we sequenced the mycobiome of soils surrounding different trees at various altitudes in the Italian Alps. To survey for yeasts species belonging to Saccharomyces genus rather than other fungal species, we performed a selectivity step involving the isolation of the internal transcribed spacer (ITS) region that is specific to this yeast group. Reads mapping to Saccharomyces species were detected in all soil samples, including reads for S. mikatae and for S. eubayanus. ITS1 alignment of the S. cerevisiae, S. paradoxus and S. kudriavzevii sequences showed up to three base pair polymorphisms with other known strains, indicating possible new lineages. Basidiomycetous fungi were still the dominant species, compared to the Ascomycota, but the selectivity step allowed for the first time the detection and study of the biodiversity of the Saccharomyces species in their natural environment.

A Probable Case of Incipient Speciation in Schizocosa Wolf Spiders Driven by Allochrony, Habitat Use, and Female Mate Choice.

There is growing evidence that speciation can occur between populations that are not geographically isolated. The emergence of assortative mating is believed to be critical to this process, but how assortative mating arises in diverging populations is poorly understood. The wolf spider genus Schizocosa has become a model system for studying mechanisms of assortative mating. We conducted a series of experiments to identify the factors that control mate pair formation in a Schizocosa population that includes both ornamented and nonornamented males. We show that the population also includes two previously unrecognized female phenotypes. One female phenotype mates mostly or exclusively with ornamented males, and the other mates mostly or exclusively with unornamented males. Assortative mating within these groups is maintained by differences in maturation time, microhabitat use, and female mate preference. We conclude that the population is not a single species, as previously believed, but rather an incipient species pair with multiple overlapping mechanisms of reproductive isolation. The identification of a new incipient species pair in the well-studied and rapidly speciating Schizocosa clade presents new opportunities for the study of speciation without geographic isolation.

Learning to speciate: The biased learning of mate preferences promotes adaptive radiation.

Bursts of rapid repeated speciation called adaptive radiations have generated much of Earth's biodiversity and fascinated biologists since Darwin, but we still do not know why some lineages radiate and others do not. Understanding what causes assortative mating to evolve rapidly and repeatedly in the same lineage is key to understanding adaptive radiation. Many species that have undergone adaptive radiations exhibit mate preference learning, where individuals acquire mate preferences by observing the phenotypes of other members of their populations. Mate preference learning can be biased if individuals also learn phenotypes to avoid in mates, and shift their preferences away from these avoided phenotypes. We used individual-based computational simulations to study whether biased and unbiased mate preference learning promotes ecological speciation and adaptive radiation. We found that ecological speciation can be rapid and repeated when mate preferences are biased, but is inhibited when mate preferences are learned without bias. Our results suggest that biased mate preference learning may play an important role in generating animal biodiversity through adaptive radiation.

Competition for resources can explain patterns of social and individual learning in nature.

In nature, animals often ignore socially available information despite the multiple theoretical benefits of social learning over individual trial-and-error learning. Using information filtered by others is quicker, more efficient and less risky than randomly sampling the environment. To explain the mix of social and individual learning used by animals in nature, most models penalize the quality of socially derived information as either out of date, of poor fidelity or costly to acquire. Competition for limited resources, a fundamental evolutionary force, provides a compelling, yet hitherto overlooked, explanation for the evolution of mixed-learning strategies. We present a novel model of social learning that incorporates competition and demonstrates that (i) social learning is favoured when competition is weak, but (ii) if competition is strong social learning is favoured only when resource quality is highly variable and there is low environmental turnover. The frequency of social learning in our model always evolves until it reduces the mean foraging success of the population. The results of our model are consistent with empirical studies showing that individuals rely less on social information where resources vary little in quality and where there is high within-patch competition. Our model provides a framework for understanding the evolution of social learning, a prerequisite for human cumulative culture.

The evolution of sexual imprinting in socially monogamous populations.

Sexual imprinting is a common mechanism of mate preference learning. It is thought to influence how traits evolve and in some cases to promote speciation. Recently there has been increasing interest in how sexual imprinting itself evolves. Theoretical work on polygynous mating systems predicts that females will evolve paternal imprinting, which means they learn to prefer phenotypes expressed by their fathers. In nature however, females of some species learn to prefer phenotypes expressed by their mothers instead. We used a dynamical systems model and tools from adaptive dynamics to study how sexual imprinting evolves in species with socially monogamous mating systems. We considered cases in which the target trait for imprinting is under viability selection but is not a reliable signal of paternal investment. Thus, the target trait signals the genetic benefits rather than the parental care benefits of mate choice. When mating is socially monogamous and there is some extra-pair paternity, we show that maternal imprinting can be favored over paternal imprinting. Counterintuitively, females often become choosier when selecting social partners in systems where extra-pair mating is more frequent. That is, females may be more selective when choosing social partners that will sire a smaller percentage of their offspring. Our results offer new testable hypotheses, and advance our understanding of the mechanisms that drive the evolution of mate choice strategies in nature.

Sexual imprinting: what strategies should we expect to see in nature?

Sexual imprinting occurs when juveniles learn mate preferences by observing the phenotypes of other members of their populations, and it is ubiquitous in nature. Imprinting strategies, that is which individuals and phenotypes are observed and how strong preferences become, vary among species. Imprinting can affect trait evolution and the probability of speciation, and different imprinting strategies are expected to have different effects. However, little is known about how and why different imprinting strategies evolve, or which strategies we should expect to see in nature. We used a mathematical model to study how the evolution of sexual imprinting depends on (1) imprinting costs and (2) the sex-specific fitness effects of the phenotype on which individuals imprint. We found that even small fixed costs prevent the evolution of sexual imprinting, but small relative costs do not. When imprinting does evolve, we identified the conditions under which females should evolve to imprint on their fathers, their mothers, or on other members of their populations. Our results provide testable hypotheses for empirical work and help to explain the conditions under which sexual imprinting might evolve to promote speciation.

Coevolution in multidimensional trait space favours escape from parasites and pathogens.

Almost all species are subject to continuous attack by parasites and pathogens. Because parasites and pathogens tend to have shorter generation times and often experience stronger selection due to interaction than their victims do, it is frequently argued that they should evolve more rapidly and thus maintain an advantage in the evolutionary race between defence and counter-defence. This prediction generates an apparent paradox: how do victim species survive and even thrive in the face of a continuous onslaught of more rapidly evolving enemies? One potential explanation is that defence is physiologically, mechanically or behaviourally easier than attack, so that evolution is less constrained for victims than for parasites or pathogens. Another possible explanation is that parasites and pathogens have enemies themselves and that victim species persist because parasites and pathogens are regulated from the top down and thus generally have only modest demographic impacts on victim populations. Here we explore a third possibility: that victim species are not as evolutionarily impotent as conventional wisdom holds, but instead have unique evolutionary advantages that help to level the playing field. We use quantitative genetic analysis and individual-based simulations to show that victims can achieve such an advantage when coevolution involves multiple traits in both the host and the parasite.

Evolution of plant-pollinator mutualisms in response to climate change.

Climate change has the potential to desynchronize the phenologies of interdependent species, with potentially catastrophic effects on mutualist populations. Phenologies can evolve, but the role of evolution in the response of mutualisms to climate change is poorly understood. We developed a model that explicitly considers both the evolution and the population dynamics of a plant-pollinator mutualism under climate change. How the populations evolve, and thus whether the populations and the mutualism persist, depends not only on the rate of climate change but also on the densities and phenologies of other species in the community. Abundant alternative mutualist partners with broad temporal distributions can make a mutualism more robust to climate change, while abundant alternative partners with narrow temporal distributions can make a mutualism less robust. How community composition and the rate of climate change affect the persistence of mutualisms is mediated by two-species Allee thresholds. Understanding these thresholds will help researchers to identify those mutualisms at highest risk owing to climate change.

Sexual dimorphism and speciation on two ecological coins: patterns from nature and theoretical predictions.

Adaptive divergence of phenotypes, such as sexual dimorphism or adaptive speciation, can result from disruptive selection via competition for limited resources. Theory indicates that speciation and sexual dimorphism can result from identical ecological conditions, but co-occurrence is unlikely because whichever evolves first should dissipate the disruptive selection necessary to drive evolution of the other. Here, we consider ecological conditions in which disruptive selection can act along multiple ecological axes. Speciation in lake populations of threespine sticklebacks (Gasterosteus aculeatus) has been attributed to disruptive selection due to competition for resources. Head shape in sticklebacks is thought to reflect adaptation to different resource acquisition strategies. We measure sexual dimorphism and species variation in head shape and body size in stickleback populations in two lakes in British Columbia, Canada. We find that sexual dimorphism in head shape is greater than interspecific differences. Using a numerical simulation model that contains two axes of ecological variation, we show that speciation and sexual dimorphism can readily co-occur when the effects of loci underlying sexually dimorphic traits are orthogonal to those underlying sexually selected traits.