Genomic landscapes of divergence among island bird populations: Evidence of parallel adaptation but at different loci?

When populations colonise new environments, they may be exposed to novel selection pressures but also suffer from extensive genetic drift due to founder effects, small population sizes and limited interpopulation gene flow. Genomic approaches enable us to study how these factors drive divergence, and disentangle neutral effects from differentiation at specific loci due to selection. Here, we investigate patterns of genetic diversity and divergence using whole-genome resequencing (>22× coverage) in Berthelot's pipit (Anthus berthelotii), a passerine endemic to the islands of three north Atlantic archipelagos. Strong environmental gradients, including in pathogen pressure, across populations in the species range, make it an excellent system in which to explore traits important in adaptation and/or incipient speciation. First, we quantify how genomic divergence accumulates across the speciation continuum, that is, among Berthelot's pipit populations, between sub species across archipelagos, and between Berthelot's pipit and its mainland ancestor, the tawny pipit (Anthus campestris). Across these colonisation timeframes (2.1 million-ca. 8000 years ago), we identify highly differentiated loci within genomic islands of divergence and conclude that the observed distributions align with expectations for non-neutral divergence. Characteristic signatures of selection are identified in loci associated with craniofacial/bone and eye development, metabolism and immune response between population comparisons. Interestingly, we find limited evidence for repeated divergence of the same loci across the colonisation range but do identify different loci putatively associated with the same biological traits in different populations, likely due to parallel adaptation. Incipient speciation across these island populations, in which founder effects and selective pressures are strong, may therefore be repeatedly associated with morphology, metabolism and immune defence.

Tests of evolutionary and genetic rescue using flour beetles, Tribolium castaneum, experimentally evolved to thermal conditions.

Small, isolated populations are often characterised by low levels of genetic diversity. This can result in inbreeding depression and reduced capacity to adapt to changes in the environment, and therefore higher risk of extinction. However, sometimes these populations can be rescued if allowed to increase in size or if migrants enter, bringing in new allelic variation and thus increasing genetic diversity. This study uses experimental manipulation of population size and migration to quantify their effects on fitness in a challenging environment to better understand genetic rescue. Using small, replicated populations of Tribolium castaneum experimentally evolved to different temperature regimes we tested genetic and demographic rescue, by performing large-scale manipulations of population size and migration and examining fitness consequences over multiple generations. We measured fitness in high temperature (38°C) thermal lines maintained at their usual 'small' population size of N = 100 individuals, and with 'large' scaled up duplicates containing N≈10,000 individuals. We compared these large lines with and without migration (m = 0.1) for 10 generations. Additionally, we assessed the effects of outcrossing at an individual level, by comparing fitness of hybrid (thermal line × stock) offspring with within-line crosses. We found that, at the population level, a rapid increase in the number of individuals in the population resulted in reduced fitness (represented by reproductive output and survival through heatwave conditions), regardless of migration. However, at an individual level, the hybrid offspring of migrants with native individuals generally demonstrated increased longevity in high temperature conditions compared with individuals from thermal selection lines. Overall, these populations showed no evidence that demographic manipulations led to genetic or evolutionary rescue. Following the effects of migration in individuals over several generations may be the next step in unravelling these conflicting results. We discuss these findings in the context of conservation intervention.

Histologic, metabolomic, and transcriptomic differences in fir trees from a peri-urban forest under chronic ozone exposure.

Urbanization modifies ecosystem conditions and evolutionary processes. This includes air pollution, mostly as tropospheric ozone (O3), which contributes to the decline of urban and peri-urban forests. A notable case are fir (Abies religiosa) forests in the peripheral mountains southwest of Mexico City, which have been severely affected by O3 pollution since the 1970s. Interestingly, some young individuals exhibiting minimal O3-related damage have been observed within a zone of significant O3 exposure. Using this setting as a natural experiment, we compared asymptomatic and symptomatic individuals of similar age (≤15 years old; n = 10) using histologic, metabolomic, and transcriptomic approaches. Plants were sampled during days of high (170 ppb) and moderate (87 ppb) O3 concentration. Given that there have been reforestation efforts in the region, with plants from different source populations, we first confirmed that all analyzed individuals clustered within the local genetic group when compared to a species-wide panel (Admixture analysis with ~1.5K SNPs). We observed thicker epidermis and more collapsed cells in the palisade parenchyma of needles from symptomatic individuals than from their asymptomatic counterparts, with differences increasing with needle age. Furthermore, symptomatic individuals exhibited lower concentrations of various terpenes (ß-pinene, ß-caryophylene oxide, α-caryophylene, and ß-α-cubebene) than asymptomatic trees, as evidenced through GC-MS. Finally, transcriptomic analyses revealed differential expression for 13 genes related to carbohydrate metabolism, plant defense, and gene regulation. Our results indicate a rapid and contrasting phenotypic response among trees, likely influenced by standing genetic variation and/or plastic mechanisms. They open the door to future evolutionary studies for understanding how O3 tolerance develops in urban environments, and how this knowledge could contribute to forest restoration.

La urbanización altera tanto las condiciones del ecosistema como los procesos evolutivos, siendo la contaminación del aire, principalmente el ozono troposférico (O3), un factor que contribuye al declive de los bosques urbanos y periurbanos. Un ejemplo destacado son los bosques de oyamel (Abies religiosa) en las montañas periféricas al suroeste de la Ciudad de México, que han sufrido graves afectaciones por la contaminación de O3 desde la década de 1970. Resulta curioso observar que algunos individuos jóvenes presentan un daño mínimo relacionado con el O3 dentro de zonas con una exposición significativa a este contaminante. Aprovechando este entorno como un experimento natural, hemos comparado individuos asintomáticos y sintomáticos de edad similar (≤15 años; n = 10) mediante enfoques histológicos, metabolómicos y transcriptómicos. Las muestras de plantas se recolectaron durante días con concentraciones altas (170 ppb) y moderadas (87 ppb) de O3. Dado que se han llevado a cabo esfuerzos de reforestación en la región con plantas de diferentes poblaciones, primero confirmamos que todos los individuos analizados se organizaron dentro del grupo genético local en comparación con un amplio panel poblacional de esta misma especie (Análisis de Admixture con ~1.5 K SNPs). Observamos una epidermis más gruesa y más células colapsadas en el parénquima en empalizada de las agujas de los individuos sintomáticos que de sus contrapartes asintomáticas, y estas diferencias aumentaban con la edad de la aguja. Además, los individuos sintomáticos exhibieron concentraciones más bajas de varios terpenos (ß­pineno, óxido de ß­cariofileno, α­cariofileno y ß­α­cubebeno) que los árboles asintomáticos, según se evidenció mediante GC­MS. Por último, los análisis transcriptómicos revelaron una expresión diferencial para trece genes relacionados con el metabolismo de carbohidratos, la defensa de plantas y la regulación génica. Nuestros resultados indican una respuesta fenotípica rápida y contrastante entre los árboles, probablemente influenciada por la variación genética presente y/o mecanismos plásticos. Estos hallazgos abren la puerta a futuros estudios evolutivos para comprender cómo se desarrolla la tolerancia al O3 en entornos urbanos y cómo este conocimiento podría contribuir a la restauración forestal.

The great tit HapMap project: A continental-scale analysis of genomic variation in a songbird.

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.

Life history correlations and trade-offs resulting from selection for dispersal in Tribolium castaneum.

Dispersal is an important facet of the life history of many organisms and is, therefore, subject to selective pressure but does not evolve in isolation. Across nature, there are examples of dispersal syndromes and life history strategies in which suites of traits coevolve and covary with dispersal in combinations that serve to maximize fitness in a given ecological context. The red rust flour beetle, Tribolium castaneum, is a model organism and globally significant post-harvest pest that relies on dispersal to reach new patches of ephemeral habitat. Dispersal behaviour in Tribolium has a strong genetic basis. However, a robust understanding of the relationship between dispersal and other life-history components, which could elucidate evolutionary processes and allow pest managers to control their spread and reduce the impact of infestation, is currently lacking. Here, we use highly replicated lines of T. castaneum previously artificially selected for divergent small-scale dispersal propensity to robustly test several important life history components: reproductive strategy, development time, and longevity. As predicted, we find that a suite of important changes as a result of our selection on dispersal: high dispersal propensity is associated with a lower number of longer mating attempts by males, lower investment in early life reproduction by females, slower development of later-laid offspring, and longer female life span. These findings indicate that correlated intraspecific variation in dispersal and related traits may represent alternative life history strategies in T. castaneum. We therefore suggest that pest management efforts to mitigate the species' agro-economic impact should consider the eco-evolutionary dynamics within multiple life histories. The benefits of doing so could be felt both through improved targeting of efforts to reduce spread and also in forecasting how the selection pressures applied through pest management are likely to affect pest evolution.

Social network centrality predicts dietary decisions in a wild bird population.

How individuals balance costs and benefits of group living remains central to understanding sociality. In relation to diet, social foraging provides many advantages but also increases competition. Nevertheless, social individuals may offset increased competition by broadening their diet and consuming novel foods. Despite the expected relationships between social behavior and dietary decisions, how sociality shapes individuals' novel food consumption remains largely untested in natural populations. Here, we use wild great tits to experimentally test how sociality predicts dietary decisions. We show that individuals with more social connections have higher propensity to use novel foods compared to socially peripheral individuals, and this is unrelated to neophobia, observations, and demographic factors. These findings indicate sociable individuals may offset potential costs of competition by foraging more broadly. We discuss how social environments may drive behavioral change in natural populations, and the implications for the causes and consequences of social strategies and dietary decisions.

Genotype-environment associations reveal genes potentially linked to avian malaria infection in populations of an endemic island bird.

Patterns of pathogen prevalence are, at least partially, the result of coevolutionary host-pathogen interactions. Thus, exploring the distribution of host genetic variation in relation to infection by a pathogen within and across populations can provide important insights into mechanisms of host defence and adaptation. Here, we use a landscape genomics approach (Bayenv) in conjunction with genome-wide data (ddRADseq) to test for associations between avian malaria (Plasmodium) prevalence and host genetic variation across 13 populations of the island endemic Berthelot's pipit (Anthus berthelotii). Considerable and consistent spatial heterogeneity in malaria prevalence was observed among populations over a period of 15 years. The prevalence of malaria infection was also strongly positively correlated with pox (Avipoxvirus) prevalence. Multiple host loci showed significant associations with malaria prevalence after controlling for genome-wide neutral genetic structure. These sites were located near to or within genes linked to metabolism, stress response, transcriptional regulation, complement activity and the inflammatory response, many previously implicated in vertebrate responses to malarial infection. Our findings identify diverse genes - not just limited to the immune system - that may be involved in host protection against malaria and suggest that spatially variable pathogen pressure may be an important evolutionary driver of genetic divergence among wild animal populations, such as Berthelot's pipit. Furthermore, our data indicate that spatio-temporal variation in multiple different pathogens (e.g. malaria and pox in this case) may have to be studied together to develop a more holistic understanding of host pathogen-mediated evolution.

The genomics of adaptation to climate in European great tit (Parus major) populations.

The recognition that climate change is occurring at an unprecedented rate means that there is increased urgency in understanding how organisms can adapt to a changing environment. Wild great tit (Parus major) populations represent an attractive ecological model system to understand the genomics of climate adaptation. They are widely distributed across Eurasia and they have been documented to respond to climate change. We performed a Bayesian genome-environment analysis, by combining local climate data with single nucleotide polymorphisms genotype data from 20 European populations (broadly spanning the species' continental range). We found 36 genes putatively linked to adaptation to climate. Following an enrichment analysis of biological process Gene Ontology (GO) terms, we identified over-represented terms and pathways among the candidate genes. Because many different genes and GO terms are associated with climate variables, it seems likely that climate adaptation is polygenic and genetically complex. Our findings also suggest that geographical climate adaptation has been occurring since great tits left their Southern European refugia at the end of the last ice age. Finally, we show that substantial climate-associated genetic variation remains, which will be essential for adaptation to future changes.

Genetic architecture of dispersal behaviour in the post-harvest pest and model organism Tribolium castaneum.

Dispersal behaviour is an important aspect of the life-history of animals. However, the genetic architecture of dispersal-related traits is often obscure or unknown, even in well studied species. Tribolium castaneum is a globally significant post-harvest pest and established model organism, yet studies of its dispersal have shown ambiguous results and the genetic basis of this behaviour remains unresolved. We combine experimental evolution and agent-based modelling to investigate the number of loci underlying dispersal in T. castaneum, and whether the trait is sex-linked. Our findings demonstrate rapid evolution of dispersal behaviour under selection. We find no evidence of sex-biases in the dispersal behaviour of the offspring of crosses, supporting an autosomal genetic basis of the trait. Moreover, simulated data approximates experimental data under simulated scenarios where the dispersal trait is controlled by one or few loci, but not many loci. Levels of dispersal in experimentally inbred lines, compared with simulations, indicate that a single locus model is not well supported. Taken together, these lines of evidence support an oligogenic architecture underlying dispersal in Tribolium castaneum. These results have implications for applied pest management and for our understanding of the evolution of dispersal in the coleoptera, the world's most species-rich order.

Runs of homozygosity reveal past bottlenecks and contemporary inbreeding across diverging populations of an island-colonizing bird.

Genomes retain evidence of the demographic history and evolutionary forces that have shaped populations and drive speciation. Across island systems, contemporary patterns of genetic diversity reflect population demography, including colonization events, bottlenecks, gene flow and genetic drift. Here, we investigate genome-wide diversity and the distribution of runs of homozygosity (ROH) using whole-genome resequencing of individuals (>22× coverage) from six populations across three archipelagos of Berthelot's pipit (Anthus berthelotii)-a passerine that has recently undergone island speciation. We show the most dramatic reduction in diversity occurs between the mainland sister species (the tawny pipit) and Berthelot's pipit and is lowest in the populations that have experienced sequential bottlenecks (i.e., the Madeiran and Selvagens populations). Pairwise sequential Markovian coalescent (PSMC) analyses estimated that Berthelot's pipit diverged from its sister species ~2 million years ago, with the Madeiran archipelago founded 50,000 years ago, and the Selvagens colonized 8000 years ago. We identify many long ROH (>1 Mb) in these most recently colonized populations. Population expansion within the last 100 years may have eroded long ROH in the Madeiran archipelago, resulting in a prevalence of short ROH (<1 Mb). However, the extensive long and short ROH detected in the Selvagens suggest strong recent inbreeding and bottleneck effects, with as much as 38% of the autosomes consisting of ROH >250 kb. These findings highlight the importance of demographic history, as well as selection and genetic drift, in shaping contemporary patterns of genomic diversity across diverging populations.

Using high-resolution contact networks to evaluate SARS-CoV-2 transmission and control in large-scale multi-day events.

The emergence of highly transmissible SARS-CoV-2 variants has created a need to reassess the risk posed by increasing social contacts as countries resume pre-pandemic activities, particularly in the context of resuming large-scale events over multiple days. To examine how social contacts formed in different activity settings influences interventions required to control Delta variant outbreaks, we collected high-resolution data on contacts among passengers and crew on cruise ships and combined the data with network transmission models. We found passengers had a median of 20 (IQR 10-36) unique close contacts per day, and over 60% of their contact episodes were made in dining or sports areas where mask wearing is typically limited. In simulated outbreaks, we found that vaccination coverage and rapid antigen tests had a larger effect than mask mandates alone, indicating the importance of combined interventions against Delta to reduce event risk in the vaccine era.

Genomic associations with poxvirus across divergent island populations in Berthelot's pipit.

Understanding the mechanisms and genes that enable animal populations to adapt to pathogens is important from an evolutionary, health and conservation perspective. Berthelot's pipit (Anthus berthelotii) experiences extensive and consistent spatial heterogeneity in avian pox infection pressure across its range of island populations, thus providing an excellent system with which to examine how pathogen-mediated selection drives spatial variation in immunogenetic diversity. Here, we test for evidence of genetic variation associated with avian pox at both an individual and population-level. At the individual level, we find no evidence that variation in MHC class I and TLR4 (both known to be important in recognising viral infection) was associated with pox infection within two separate populations. However, using genotype-environment association (Bayenv) in conjunction with genome-wide (ddRAD-seq) data, we detected strong associations between population-level avian pox prevalence and allele frequencies of single nucleotide polymorphisms (SNPs) at a number of sites across the genome. These sites were located within genes involved in cellular stress signalling and immune responses, many of which have previously been associated with responses to viral infection in humans and other animals. Consequently, our analyses indicate that pathogen-mediated selection may play a role in shaping genomic variation among relatively recently colonised island bird populations and highlight the utility of genotype-environment associations for identifying candidate genes potentially involved in host-pathogen interactions.

Telomere heritability and parental age at conception effects in a wild avian population.

Individual variation in telomere length is predictive of health and mortality risk across a range of species. However, the relative influence of environmental and genetic variation on individual telomere length in wild populations remains poorly understood. Heritability of telomere length has primarily been calculated using parent-offspring regression which can be confounded by shared environments. To control for confounding variables, quantitative genetic "animal models" can be used, but few studies have applied animal models in wild populations. Furthermore, parental age at conception may also influence offspring telomere length, but most studies have been cross-sectional. We investigated within- and between-parental age at conception effects and heritability of telomere length in the Seychelles warbler using measures from birds caught over 20 years and a multigenerational pedigree. We found a weak negative within-paternal age at conception effect (as fathers aged, their offspring had shorter telomeres) and a weak positive between-maternal age at conception effect (females that survived to older ages had offspring with longer telomeres). Animal models provided evidence that heritability and evolvability of telomere length were low in this population, and that variation in telomere length was not driven by early-life effects of hatch period or parental identities. Quantitative polymerase chain reaction plate had a large influence on telomere length variation and not accounting for it in the models would have underestimated heritability. Our study illustrates the need to include and account for technical variation in order to accurately estimate heritability, as well as other environmental effects, on telomere length in natural populations.

Causes and consequences of telomere lengthening in a wild vertebrate population.

Telomeres have been advocated to be important markers of biological age in evolutionary and ecological studies. Telomeres usually shorten with age and shortening is frequently associated with environmental stressors and increased subsequent mortality. Telomere lengthening - an apparent increase in telomere length between repeated samples from the same individual - also occurs. However, the exact circumstances, and consequences, of telomere lengthening are poorly understood. Using longitudinal data from the Seychelles warbler (Acrocephalus sechellensis), we tested whether telomere lengthening - which occurs in adults of this species - is associated with specific stressors (reproductive effort, food availability, malarial infection and cooperative breeding) and predicts subsequent survival. In females, telomere shortening was observed under greater stress (i.e., low food availability, malaria infection), while telomere lengthening was observed in females experiencing lower stress (i.e., high food availability, assisted by helpers, without malaria). The telomere dynamics of males were not associated with the key stressors tested. These results indicate that, at least for females, telomere lengthening occurs in circumstances more conducive to self-maintenance. Importantly, both females and males with lengthened telomeres had improved subsequent survival relative to individuals that displayed unchanged, or shortened, telomeres - indicating that telomere lengthening is associated with individual fitness. These results demonstrate that telomere dynamics are bidirectionally responsive to the level of stress that an individual faces, but may poorly reflect the accumulation of stress over an individuals lifetime.

Genomic variation, population history and within-archipelago adaptation between island bird populations.

Oceanic island archipelagos provide excellent models to understand evolutionary processes. Colonization events and gene flow can interact with selection to shape genetic variation at different spatial scales. Landscape-scale variation in biotic and abiotic factors may drive fine-scale selection within islands, while long-term evolutionary processes may drive divergence between distantly related populations. Here, we examine patterns of population history and selection between recently diverged populations of the Berthelot's pipit (Anthus berthelotii), a passerine endemic to three North Atlantic archipelagos. First, we use demographic trees and f3 statistics to show that genome-wide divergence across the species range is largely shaped by colonization and bottlenecks, with evidence of very weak gene flow between populations. Then, using a genome scan approach, we identify signatures of divergent selection within archipelagos at single nucleotide polymorphisms (SNPs) in genes potentially associated with craniofacial development and DNA repair. We did not detect within-archipelago selection at the same SNPs as were detected previously at broader spatial scales between archipelagos, but did identify signatures of selection at loci associated with similar biological functions. These findings suggest that similar ecological factors may repeatedly drive selection between recently separated populations, as well as at broad spatial scales across varied landscapes.

Tribolium beetles as a model system in evolution and ecology.

Flour beetles of the genus Tribolium have been utilised as informative study systems for over a century and contributed to major advances across many fields. This review serves to highlight the significant historical contribution that Tribolium study systems have made to the fields of ecology and evolution, and to promote their use as contemporary research models. We review the broad range of studies employing Tribolium to make significant advances in ecology and evolution. We show that research using Tribolium beetles has contributed a substantial amount to evolutionary and ecological understanding, especially in the fields of population dynamics, reproduction and sexual selection, population and quantitative genetics, and behaviour, physiology and life history. We propose a number of future research opportunities using Tribolium, with particular focus on how their amenability to forward and reverse genetic manipulation may provide a valuable complement to other insect models.

Comparative genomics analyses indicate differential methylated amine utilization trait within members of the genus Gemmobacter.

Methylated amines are ubiquitous in the environment and play a role in regulating the earth's climate via a set of complex biological and chemical reactions. Microbial degradation of these compounds is thought to be a major sink. Recently we isolated a facultative methylotroph, Gemmobacter sp. LW-1, an isolate from the unique environment Movile Cave, Romania, which is capable of methylated amine utilization as a carbon source. Here, using a comparative genomics approach, we investigate how widespread methylated amine utilization is within members of the bacterial genus Gemmobacter. Seven genomes of different Gemmobacter species isolated from diverse environments, such as activated sludge, fresh water, sulphuric cave waters (Movile Cave) and the marine environment were available from the public repositories and used for the analysis. Our results indicate that methylamine utilization is a distinctive feature of selected members of the genus Gemmobacter, namely G. aquatilis, G. lutimaris, G. sp. HYN0069, G. caeni and G. sp. LW-1 have the genetic potential while others (G. megaterium and G. nectariphilus) have not.

Genetic pest management and the background genetics of release strains.

Genetic pest management (GPM) methods involve releasing modified versions of a pest species to mate with wild pests in the target area. Proposed for a wide range of applications in public health, agriculture and conservation, most progress has been made with pest insects. Offspring of the released modified insects and wild pests carry the modification-which might be transgenes, artificially introduced Wolbachia or genetic damage from radiation, for example-but they also carry a complete haploid genome from their laboratory-reared parent, as well as one from their wild parent. Unless these F1 hybrids are completely unable to reproduce, further mating will lead to introgression of DNA sequences from the release strain into the wild population. We discuss issues around strain selection and the potential consequences of such introgression. We conclude that such introgression is probably harmless in almost all circumstances, and could, in theory, provide specific additional benefits to the release programme. We outline population monitoring approaches that could be used, going forward, to determine how background genetics may affect GPM. This article is part of the theme issue 'Novel control strategies for mosquito-borne diseases'.

Polyandry provides reproductive and genetic benefits in colonising populations.

Polyandry, when females mate with more than one male, is theorised to play an important role in successful colonisation of new habitats. In addition to possible benefits from sexual selection, even mild polyandry could facilitate colonisation by protecting against inbreeding and reducing the costs of mating with incompatible or infertile males. Here, we measure the importance of mild polyandry for population viability and reproductive fitness following experimental founder events into a higher-temperature regime. Using colonisation experiments with the model beetle Tribolium castaneum, in which females can produce offspring for up to 140 days following a single mating, we founded more than 100 replicate populations using single females that had been given the opportunity to mate with either one or two males and then tracked their subsequent population dynamics. Following population viability and fitness across 10 generations, we found that extinction rates were significantly lower in populations founded by females given polyandrous opportunities to mate with two males (9%) compared to populations founded by monogamous females (34%). In addition, populations founded by females that had been provided with opportunities to store sperm from two different males showed double the median productivity following colonisation compared to monogamous-founded populations. Notably, we identified short-term and longer-term benefits to post-colonisation populations from double-mating, with results suggesting that polyandry acts to both protect against mating with incompatible males through the founder event, and reduce inbreeding depression as the colonisation proceeds for 10 generations. Our results therefore show that even mild polyandry provides both reproductive and genetic benefits for colonising populations.

Temporal dynamics of competitive fertilization in social groups of red junglefowl (Gallus gallus) shed new light on avian sperm competition.

Studies of birds have made a fundamental contribution to elucidating sperm competition processes, experimentally demonstrating the role of individual mechanisms in competitive fertilization. However, the relative importance of these mechanisms and the way in which they interact under natural conditions remain largely unexplored. Here, we conduct a detailed behavioural study of freely mating replicate groups of red junglefowl, Gallus gallus, to predict the probability that competing males fertilize individual eggs over the course of 10-day trials. Remating frequently with a female and mating last increased a male's probability of fertilization, but only for eggs ovulated in the last days of a trial. Conversely, older males, and those mating with more polyandrous females, had consistently lower fertilization success. Similarly, resistance to a male's mating attempts, particularly by younger females, reduced fertilization probability. After considering these factors, male social status, partner relatedness and the estimated state of male extragonadal sperm reserves did not predict sperm competition outcomes. These results shed new light on sperm competition dynamics in taxa such as birds, with prolonged female sperm storage and staggered fertilizations. This article is part of the theme issue 'Fifty years of sperm competition'.