RESUMEN
A major aim of evolutionary biology is to understand why patterns of genomic diversity vary within taxa and space. Large-scale genomic studies of widespread species are useful for studying how environment and demography shape patterns of genomic divergence. Here, we describe one of the most geographically comprehensive surveys of genomic variation in a wild vertebrate to date; the great tit (Parus major) HapMap project. We screened ca 500,000 SNP markers across 647 individuals from 29 populations, spanning ~30 degrees of latitude and 40 degrees of longitude - almost the entire geographical range of the European subspecies. Genome-wide variation was consistent with a recent colonisation across Europe from a South-East European refugium, with bottlenecks and reduced genetic diversity in island populations. Differentiation across the genome was highly heterogeneous, with clear 'islands of differentiation', even among populations with very low levels of genome-wide differentiation. Low local recombination rates were a strong predictor of high local genomic differentiation (FST), especially in island and peripheral mainland populations, suggesting that the interplay between genetic drift and recombination causes highly heterogeneous differentiation landscapes. We also detected genomic outlier regions that were confined to one or more peripheral great tit populations, probably as a result of recent directional selection at the species' range edges. Haplotype-based measures of selection were related to recombination rate, albeit less strongly, and highlighted population-specific sweeps that likely resulted from positive selection. Our study highlights how comprehensive screens of genomic variation in wild organisms can provide unique insights into spatio-temporal evolutionary dynamics.
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Variación Genética , Polimorfismo de Nucleótido Simple , Pájaros Cantores , Animales , Pájaros Cantores/genética , Pájaros Cantores/clasificación , Genética de Población/métodos , Europa (Continente) , Passeriformes/genética , Passeriformes/clasificación , Haplotipos/genética , Recombinación Genética , Selección GenéticaRESUMEN
Understanding the evolution of coral endosymbiosis requires a predictive framework that integrates life-history theory and ecology with cell biology. The time has come to bridge disciplines and use a model systems approach to achieve this aim.
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Antozoos , Animales , Antozoos/genética , Simbiosis , Ecología , Arrecifes de Coral , Evolución BiológicaRESUMEN
Vocal rhythm plays a fundamental role in sexual selection and species recognition in birds, but little is known of its genetic basis due to the confounding effect of vocal learning in model systems. Uncovering its genetic basis could facilitate identifying genes potentially important in speciation. Here we investigate the genomic underpinnings of rhythm in vocal non-learning Pogoniulus tinkerbirds using 135 individual whole genomes distributed across a southern African hybrid zone. We find rhythm speed is associated with two genes that are also known to affect human speech, Neurexin-1 and Coenzyme Q8A. Models leveraging ancestry reveal these candidate loci also impact rhythmic stability, a trait linked with motor performance which is an indicator of quality. Character displacement in rhythmic stability suggests possible reinforcement against hybridization, supported by evidence of asymmetric assortative mating in the species producing faster, more stable rhythms. Because rhythm is omnipresent in animal communication, candidate genes identified here may shape vocal rhythm across birds and other vertebrates.
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Vocalización Animal , Animales , Vocalización Animal/fisiología , Masculino , Genómica , Genoma/genética , Femenino , Pájaros Cantores/genética , Pájaros Cantores/fisiología , Aves/genética , Aves/fisiologíaRESUMEN
Closer integration between behavioral ecology and quantitative genetics has resulted in a recent increase in studies partitioning sources of variation in labile traits. Repeatable between-individual differences are commonly documented, and their existence is generally explained using adaptive arguments, implying that selection has shaped variation at the among- and within-individual level. However, predicting the expected pattern of non-adaptive phenotypic variation around an optimal phenotypic value is difficult, hampering our ability to provide quantitative assessments of the adaptive nature of observed patterns of phenotypic variation within a population. We argue that estimating the strength of selection on trait variation among and within individuals provides a way to test adaptive theory concerned with phenotypic variation. To achieve this aim, we describe a nonlinear selection analysis that enables the study of the selective pressures on trait means and their among- and within-individual variation. By describing an integrative approach for studying the strength of selection on phenotypic variation at different levels, we hope to stimulate empirical studies investigating the ecological factors that can shape the repeatability, heritability, and coefficients of variation of labile and other repeatedly expressed traits.
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Evolución Biológica , Variación Genética , Humanos , FenotipoRESUMEN
Ticks are important vectors of human and animal pathogens, but many questions remain unanswered regarding their taxonomy. Molecular sequencing methods have allowed research to start understanding the evolutionary history of even closely related tick species. Ixodes inopinatus is considered a sister species and highly similar to Ixodes ricinus, an important vector of many tick-borne pathogens in Europe, but identification between these species remains ambiguous with disagreement on the geographic extent of I. inopinatus. In 2018-2019, 1583 ticks were collected from breeding great tits (Parus major) in southern Germany, of which 45 were later morphologically identified as I. inopinatus. We aimed to confirm morphological identification using molecular tools. Utilizing two genetic markers (16S rRNA, TROSPA) and whole genome sequencing of specific ticks (n = 8), we were able to determine that German samples, morphologically identified as I. inopinatus, genetically represent I. ricinus regardless of previous morphological identification, and most likely are not I. ricinus/I. inopinatus hybrids. Further, our results showed that the entire mitochondrial genome, let alone singular mitochondrial genes (i.e., 16S), is unable to distinguish between I. ricinus and I. inopinatus. Our results suggest that I. inopinatus is geographically isolated as a species (northern Africa and potentially southern Spain and Portugal) and brings into question whether I. inopinatus exists in central Europe. Our results highlight the probable existence of I. inopinatus and the power of utilizing genomic data in answering questions regarding tick taxonomy.
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Ixodes , Humanos , Animales , Ixodes/genética , ARN Ribosómico 16S/genética , Europa (Continente) , Alemania , PortugalRESUMEN
A major question in behavioural ecology is why behaviour, physiology and morphology are often integrated into syndromes. In great tits, Parus major, for example, explorative males are larger (vs. smaller) and leaner (vs. heavier) compared to less explorative individuals. Unfortunately, considerable debate exists on whether patterns found in specific studies are replicable. This debate calls for study replication among species, populations and sexes. We measured behavioural (exploration), physiological (breathing rate) and morphological traits (body mass, tarsus length, wing length, bill length) in two species (great vs. blue tits Cyanistes caeruleus), two populations (Forstenrieder Park vs. Starnberg) and two sexes (males vs. females). We then tested whether the same pattern of integration characterized all unique combinations of these three biological categories (hereafter called datasets). We used a multi-year repeated measures set-up to estimate among-individual trait correlation matrices for each dataset. We then used structural equation modelling to test for size-dependent behaviour and physiology, size-corrected (i.e. size-independent) behaviour-physiology correlations and size-corrected body mass-dependent behaviour and physiology. Finally, we used meta-analyses to test which structural paths were generally (vs. conditionally) supported (vs. unsupported). We found general and consistent support for size-dependent physiology and size-corrected body mass-dependent physiology across datasets: faster breathers were smaller but heavier for their size. Unexpectedly, condition-dependent behaviour was not supported: explorative birds were neither leaner, nor was this relationship heterogeneous across datasets. All other hypothesized patterns were dataset-specific: the covariance between size and behaviour, and between behaviour and physiology differed in sign between datasets, and both were, on average, not supported. This heterogeneity was not explained by any of our moderators: species, population or sex. The specific pattern of size- and condition-dependent physiology reported for a unique combination of species, population, and sex, thus generally predicted those in others. Patterns of size- or condition-dependent behaviour (i.e. 'personality'), or behaviour-physiology syndromes reported in specific datasets, by contrast, did not. These findings call for studies revealing the ecological background of this variation and highlight the value of study replication to help understand whether patterns of phenotypic integration reported in one study can be generalized.
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Passeriformes , Pájaros Cantores , Masculino , Femenino , Animales , Síndrome , Personalidad , Conducta Animal/fisiología , Passeriformes/fisiología , Pájaros Cantores/fisiologíaRESUMEN
Social evolution and the dynamics of social interactions have previously been studied under the frameworks of quantitative genetics and behavioural ecology. In quantitative genetics, indirect genetic effects of social partners on the socially plastic phenotypes of focal individuals typically lack crucial detail already included in treatments of social plasticity in behavioural ecology. Specifically, whilst focal individuals (e.g. receivers) may show variation in their 'responsiveness' to the social environment, individual social partners (e.g. signallers) may have a differential 'impact' on focal phenotypes. Here we propose an integrative framework, that highlights the distinction between responsiveness versus impact in indirect genetic effects for a range of behavioural traits. We describe impact and responsiveness using a reaction norm approach and provide statistical models for the assessment of these effects of focal and social partner identity in different types of social interactions. By providing such a framework, we hope to stimulate future quantitative research investigating the causes and consequences of social interactions on phenotypic evolution.
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Individualidad , Conducta Social , Animales , Conducta Animal , Fenotipo , Medio Social , Evolución BiológicaRESUMEN
Learning is a familiar process to most people, but it currently lacks a fully developed theoretical position within evolutionary biology. Learning (memory and forgetting) involves adjustments in behaviour in response to cumulative sequences of prior experiences or exposures to environmental cues. We therefore suggest that all forms of learning (and some similar biological phenomena in development, aging, acquired immunity and acclimation) can usefully be viewed as special cases of phenotypic plasticity, and formally modelled by expanding the concept of reaction norms to include additional environmental dimensions quantifying sequences of cumulative experience (learning) and the time delays between events (forgetting). Memory therefore represents just one of a number of different internal neurological, physiological, hormonal and anatomical 'states' that mediate the carry-over effects of cumulative environmental experiences on phenotypes across different time periods. The mathematical and graphical conceptualisation of learning as plasticity within a reaction norm framework can easily accommodate a range of different ecological scenarios, closely linking statistical estimates with biological processes. Learning and non-learning plasticity interact whenever cumulative prior experience causes a modification in the reaction norm (a) elevation [mean phenotype], (b) slope [responsiveness], (c) environmental estimate error [informational memory] and/or (d) phenotypic precision [skill acquisition]. Innovation and learning new contingencies in novel (laboratory) environments can also be accommodated within this approach. A common reaction norm approach should thus encourage productive cross-fertilisation of ideas between traditional studies of learning and phenotypic plasticity. As an example, we model the evolution of plasticity with and without learning under different levels of environmental estimation error to show how learning works as a specific adaptation promoting phenotypic plasticity in temporally autocorrelated environments. Our reaction norm framework for learning and analogous biological processes provides a conceptual and mathematical structure aimed at usefully stimulating future theoretical and empirical investigations into the evolution of plasticity across a wider range of ecological contexts, while providing new interdisciplinary connections regarding learning mechanisms.
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Adaptación Fisiológica , Evolución Biológica , Aclimatación , Humanos , FenotipoRESUMEN
Predictable behaviour (or 'behavioural stability') might be favoured in certain ecological contexts, for example when representing a quality signal. Costs associated with producing stable phenotypes imply selection should favour plasticity in stability when beneficial. Repeatable among-individual differences in degree of stability are simultaneously expected if individuals differ in ability to pay these costs, or in how they resolve cost-benefit trade-offs. Bird song represents a prime example, where stability may be costly yet beneficial when stable singing is a quality signal favoured by sexual selection. Assuming energetic costs, ecological variation (e.g. in food availability) should result in both within- and among-individual variation in stability. If song stability represents a quality signal, we expect directional selection favouring stable singers. For a 3-year period, we monitored 12 nest box plots of great tits Parus major during breeding. We recorded male songs during simulated territory intrusions, twice during their mate's laying stage and twice during incubation. Each preceding winter, we manipulated food availability. Assuming that stability is costly, we expected food-supplemented males to sing more stable songs. We also expected males to sing more stable songs early in the breeding season (when paternity is not decided) and stable singers to have increased reproductive success. We found strong support for plasticity in stability for two key song characteristics: minimum frequency and phrase length. Males were plastic because they became more stable over the season, contrary to expectations. Food supplementation did not affect body condition but increased stability in minimum frequency. This treatment effect occurred only in 1 year, implying that food supplementation affected stability only in interaction with (unknown) year-specific ecological factors. We found no support for directional, correlational or fluctuating selection on the stability in minimum frequency (i.e. the song trait whose stability exhibited cross-year repeatability): stable singers did not have higher reproductive success. Our findings imply that stability in minimum frequency is not a fitness quality indicator unless males enjoy fitness benefits via pathways not studied here. Future studies should thus address the mechanisms shaping and maintaining individual repeatability of song stability in the wild.
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Passeriformes , Pájaros Cantores , Animales , Animales Salvajes , Masculino , Reproducción , Estaciones del AñoRESUMEN
Assortative mating occurs when paired individuals of the same population are more similar than expected by chance. This form of non-random assortment has long been predicted to play a role in many evolutionary processes because assortatively mated individuals are assumed to be genetically similar. However, this assumption may always hold for labile traits, or traits that are measured with error. For such traits, there is a variety of proximate mechanisms that can drive phenotypic resemblance between mated partners that, notably, have very different evolutionary repercussions. Bettering our understanding of the role of assortative mating in evolution will thus require insight into its proximate causes. To date, empirical research remains sparse, especially when for labile traits. This special issue aims to stimulate such research while promoting the usage and development of statistical approaches allowing the quantification of the relative roles of alternative proximate mechanisms causing assortative mating. To this end, we first describe how the phenotypic covariance between mated partners can be usefully partitioned into components that capture one or several of five distinct mechanisms. We then demonstrate why the importance of mechanisms causing genetic covariance between the traits of partners may often be overestimated. Finally, we detail how the evolutionary causes and consequences of the diverse mechanisms may be identified.
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Reproducción , Humanos , FenotipoRESUMEN
There is considerable debate about the occurrence of assortative mating between phenotypic traits measured within natural populations. Meta-analyses have implied that assortative mating occurs generally in natural populations, but recent work indicates these conclusions largely result from biased data. Specifically, estimates of phenotypic correlations between mating partners do not solely result from nonrandom associations between individual-level traits of partners but also from other biological processes (joint phenotypic plasticity, indirect genetic effects), methodological practices (observer bias) and other unexplained residual correlations (e.g. correlated measurement error). This paper puts this critique to test. First, we estimated the overall phenotypic correlation between phenotypic traits of mating partners for a wild population of great tits. Second, we estimated various key variance components to reveal the extent to which phenotypic correlations between partners resulted from assortative mating, reversible plasticity, social partner effects and methodological practices. We performed our analyses for a range of phenotypic traits (body mass, breathing rate, exploration behaviour, wing and tarsus length) to derive general conclusions not hinging on the specifics of the traits involved. Our analyses support the conclusion that patterns of assortative mating exist at first glance but occur because of the biasing effects of correlated residuals likely caused by a combination of phenotypic responses to unknown environmental factors or measurement error-not because of intrinsic patterns of assortative mating.
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Passeriformes , Animales , Passeriformes/genética , Fenotipo , ReproducciónRESUMEN
Heterogeneous selection is often proposed as a key mechanism maintaining repeatable behavioral variation ("animal personality") in wild populations. Previous studies largely focused on temporal variation in selection within single populations. The relative importance of spatial versus temporal variation remains unexplored, despite these processes having distinct effects on local adaptation. Using data from >3,500 great tits (Parus major) and 35 nest box plots situated within five West-European populations monitored over 4 to 18 y, we show that selection on exploration behavior varies primarily spatially, across populations, and study plots within populations. Exploration was, simultaneously, selectively neutral in the average population and year. These findings imply that spatial variation in selection may represent a primary mechanism maintaining animal personalities, likely promoting the evolution of local adaptation, phenotype-dependent dispersal, and nonrandom settlement. Selection also varied within populations among years, which may counteract local adaptation. Our study underlines the importance of combining multiple spatiotemporal scales in the study of behavioral adaptation.
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Migración Animal/fisiología , Conducta Exploratoria/fisiología , Passeriformes/fisiología , Animales , Europa (Continente) , Dinámicas no LinealesRESUMEN
Urbanisation is increasing worldwide, and there is now ample evidence of phenotypic changes in wild organisms in response to this novel environment. Yet, the genetic changes and genomic architecture underlying these adaptations are poorly understood. Here, we genotype 192 great tits (Parus major) from nine European cities, each paired with an adjacent rural site, to address this major knowledge gap in our understanding of wildlife urban adaptation. We find that a combination of polygenic allele frequency shifts and recurrent selective sweeps are associated with the adaptation of great tits to urban environments. While haplotypes under selection are rarely shared across urban populations, selective sweeps occur within the same genes, mostly linked to neural function and development. Collectively, we show that urban adaptation in a widespread songbird occurs through unique and shared selective sweeps in a core-set of behaviour-linked genes.
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Adaptación Fisiológica/genética , Evolución Molecular , Passeriformes/fisiología , Selección Genética , Urbanización , Distribución Animal , Animales , Ciudades , Europa (Continente) , Frecuencia de los GenesRESUMEN
Despite increasing evidence of the importance of repeatable among-individual differences in behaviour (animal personality) in ecology and evolution, little remains known about the role of animal personalities in sexual selection. Here, we present an investigation of the hypothesis that the personalities of individuals and their sexual partners play a role in different episodes of sexual selection, and the extent to which these effects are modulated by the social environment. We first examined how two repeatable behaviours-exploration and boldness-are associated with pre- and postcopulatory sexual selection in male red junglefowl Gallus gallus, using replicate groups across three experimental sex ratio treatments. We further explored how the social environment modulates relationships between male personality and mating performance, and whether mating is assortative or disassortative with respect to exploration or boldness. Finally, we examined behavioural mechanisms linking personality with mating performance. Across all sex ratios, the fastest and slowest exploring males courted females proportionally less, and faster exploring males associated with females more and received more sexual solicitations. In female-biased groups, the fastest and slowest exploring males experienced the highest mating success and lowest sperm competition intensity. Faster exploring males also obtained more mates in female-biased groups when their competitors were, on average, slower exploring, and the proportion of matings obtained by fast-exploring males decreased with the proportion of fast-exploring males in a group, consistent with negative frequency-dependent sexual selection. While boldness did not predict mating performance, there was a tendency for individuals to mate disassortatively with respect to boldness. Collectively, our results suggest that male exploration can play a role in sexual selection, and that sexual selection on personality is complex and contingent on the social environment.
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Preferencia en el Apareamiento Animal , Animales , Pollos , Femenino , Masculino , Personalidad , Conducta Sexual Animal , Selección SexualRESUMEN
In Focus: Dhellemmes, F., Finger J.S., Smukall M.J., Gruber S.H., Guttridge T.L., Laskowski K.L., & J. Krause. (2020) Personality-driven life-history trade-offs differ in two subpopulations of free-ranging predators. Journal of Animal Ecology, 90, 260-272. Life-history theory predicts that explorative individuals live-fast-but-die-young as they take risks to rapidly accumulate resources. Dhellemmes et al. (2020) show that fast-exploring sharks forage in risky habitats, where they grow-fast-but-die-young. In higher risk environments, however, this personality-related pace-of-life-syndrome does not exist because neither fast- nor slow-exploring types venture out into risky areas. The study thereby reveals the key role of ecology as a mediator of personality-related pace-of-life-syndromes in the wild.
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Rasgos de la Historia de Vida , Tiburones , Animales , Ecosistema , Aprendizaje , PersonalidadRESUMEN
The integration and synthesis of the data in different areas of science is drastically slowed and hindered by a lack of standards and networking programmes. Long-term studies of individually marked animals are not an exception. These studies are especially important as instrumental for understanding evolutionary and ecological processes in the wild. Furthermore, their number and global distribution provides a unique opportunity to assess the generality of patterns and to address broad-scale global issues (e.g. climate change). To solve data integration issues and enable a new scale of ecological and evolutionary research based on long-term studies of birds, we have created the SPI-Birds Network and Database (www.spibirds.org)-a large-scale initiative that connects data from, and researchers working on, studies of wild populations of individually recognizable (usually ringed) birds. Within year and a half since the establishment, SPI-Birds has recruited over 120 members, and currently hosts data on almost 1.5 million individual birds collected in 80 populations over 2,000 cumulative years, and counting. SPI-Birds acts as a data hub and a catalogue of studied populations. It prevents data loss, secures easy data finding, use and integration and thus facilitates collaboration and synthesis. We provide community-derived data and meta-data standards and improve data integrity guided by the principles of Findable, Accessible, Interoperable and Reusable (FAIR), and aligned with the existing metadata languages (e.g. ecological meta-data language). The encouraging community involvement stems from SPI-Bird's decentralized approach: research groups retain full control over data use and their way of data management, while SPI-Birds creates tailored pipelines to convert each unique data format into a standard format. We outline the lessons learned, so that other communities (e.g. those working on other taxa) can adapt our successful model. Creating community-specific hubs (such as ours, COMADRE for animal demography, etc.) will aid much-needed large-scale ecological data integration.
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Aves , Metadatos , Animales , Bases de Datos FactualesRESUMEN
When individuals are measured more than once in the same context they do not behave in exactly the same way each time. The degree of predictability differs between individuals, with some individuals showing low levels of variation around their behavioural mean while others show high levels of variation. This intra-individual variability in behaviour has received much less attention than between-individual variability in behaviour, and very little is known about the underlying mechanisms that affect this potentially large but understudied component of behavioural variation. In this study, we combine standardized behavioural tests in a chicken intercross to estimate intra-individual behavioural variability with a large-scale genomics analysis to identify genes affecting intra-individual behavioural variability in an avian population. We used a variety of different anxiety-related behavioural phenotypes for this purpose. Our study shows that intra-individual variability in behaviour has a direct genetic basis that is largely unique compared to the genetic architecture for the standard behavioural measures they are based on (at least in the detected quantitative trait locus). We identify six suggestive candidate genes that may underpin differences in intra-individual behavioural variability, with several of these candidates having previously been linked to behaviour and mental health. These findings demonstrate that intra-individual variability in behaviour appears to be a heritable trait in and of itself on which evolution can act.
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Conducta Animal/fisiología , Variación Biológica Individual , Pollos/genética , Regulación de la Expresión Génica , Sitios de Carácter Cuantitativo , Animales , Femenino , Genómica , Masculino , FenotipoRESUMEN
Animal tracking and biologging devices record large amounts of data on individual movement behaviors in natural environments. In these data, movement ecologists often view unexplained variation around the mean as "noise" when studying patterns at the population level. In the field of behavioral ecology, however, focus has shifted from population means to the biological underpinnings of variation around means. Specifically, behavioral ecologists use repeated measures of individual behavior to partition behavioral variability into intrinsic among-individual variation and reversible behavioral plasticity and to quantify: a) individual variation in behavioral types (i.e. different average behavioral expression), b) individual variation in behavioral plasticity (i.e. different responsiveness of individuals to environmental gradients), c) individual variation in behavioral predictability (i.e. different residual within-individual variability of behavior around the mean), and d) correlations among these components and correlations in suites of behaviors, called 'behavioral syndromes'. We here suggest that partitioning behavioral variability in animal movements will further the integration of movement ecology with other fields of behavioral ecology. We provide a literature review illustrating that individual differences in movement behaviors are insightful for wildlife and conservation studies and give recommendations regarding the data required for addressing such questions. In the accompanying R tutorial we provide a guide to the statistical approaches quantifying the different aspects of among-individual variation. We use movement data from 35 African elephants and show that elephants differ in a) their average behavior for three common movement behaviors, b) the rate at which they adjusted movement over a temporal gradient, and c) their behavioral predictability (ranging from more to less predictable individuals). Finally, two of the three movement behaviors were correlated into a behavioral syndrome (d), with farther moving individuals having shorter mean residence times. Though not explicitly tested here, individual differences in movement and predictability can affect an individual's risk to be hunted or poached and could therefore open new avenues for conservation biologists to assess population viability. We hope that this review, tutorial, and worked example will encourage movement ecologists to examine the biology of individual variation in animal movements hidden behind the population mean.
RESUMEN
Although mating represents a mutual interaction, the study of mate preferences has long focused on choice in one sex and preferred traits in the other. This has certainly been the case in the study of the costs and condition-dependent expression of mating preferences, with the majority of studies concerning female preference. The condition dependence and genetic architecture of mutual mate preferences remain largely unstudied, despite their likely relevance for the evolution of preferences and of mating behavior more generally. Here we measured (a) male and female mate preferences and (b) intersexual genetic correlations for the mating activity in pedigreed populations of southern field crickets (Gryllus bimaculatus) raised on a favorable (free-choice) or a stressful (protein-deprived) diet. In the favorable dietary environment, mutual mate preferences were strong, and the intersexual genetic covariance for mating activity was not different from one. However, in the stressful dietary environment, mutual mate preferences were weak, and the intersexual genetic covariance for mating activity was significantly smaller than one. Altogether, our results show that diet environments affect the expression of genetic variation in mating behaviors: when the environment is stressful, both (a) the strength of mutual mate preference and (b) intersexual genetic covariance for mating activity tend to be weaker. This implies that mating dynamics strongly vary across environments.