Genetic patterns reveal geographic drivers of divergence in silvereyes (Zosterops lateralis).

Identifying mechanisms that drive population divergence under varying geographic and ecological scenarios can inform our understanding of evolution and speciation. In particular, analysis of genetic data from island populations with known colonisation timelines allows us to identify potential source populations of diverging island subspecies and current relationships among populations. Silvereyes (Zosterops lateralis) are a small passerine that have served as a valuable study system to investigate evolutionary patterns on both large and small geographic scales. We examined genetic relatedness and diversity of two silvereye subspecies, the mainland Z. l. cornwalli and island Z. l. chlorocephalus, and used 18 077 single nucleotide polymorphisms (SNPs), to compare locations across southeast Queensland, Australia. Although silvereyes are prolific island colonisers our findings revealed population divergence over relatively small spatial scales was strongly influenced by geographic isolation mediated by water barriers. Strong genetic connectivity was displayed between mainland sites, but minimal inter-island connectivity was shown despite comparable sampling distances. Genetic diversity analysis showed little difference in heterozygosity between island and mainland populations, but lower inbreeding scores among the island populations. Our study confirmed the range of the Z. l. chlorocephalus subspecies throughout the southern Great Barrier Reef. Our results show that water barriers and not geographic distance per se are important in driving incipient divergence in island populations. This helps to explain the relatively high number of phenotypically differentiated, but often geographically proximate, island silvereye subspecies compared to a lower number of phenotypically less well-defined Australian continental subspecies.

Integration of population genetics with oceanographic models reveals strong connectivity among coral reefs across Seychelles.

Many countries with tropical reef systems face hard choices preserving coral reefs in the face of climate change on limited budgets. One approach to maximising regional reef resilience is targeting management efforts and resources at reefs that export large numbers of larvae to other reefs. However, this requires reef connectivity to be quantified. To map coral connectivity in the Seychelles reef system we carried out a population genomic study of the Porites lutea species complex using 241 sequenced colonies from multiple islands. To identify oceanographic drivers of this connectivity and quantify variability, we further used a 2 km resolution regional ocean simulation coupled with a larval dispersal model to predict the flow of coral larvae between reef sites. Patterns of admixture and gene flow are broadly supported by model predictions, but the realised connectivity is greater than that predicted from model simulations. Both methods detected a biogeographic dispersal barrier between the Inner and Outer Islands of Seychelles. However, this barrier is permeable and substantial larval transport is possible across Seychelles, particularly for one of two putative species found in our genomic study. The broad agreement between predicted connectivity and observed genetic patterns supports the use of such larval dispersal simulations in reef system management in Seychelles and the wider region.

Long-insert sequence capture detects high copy numbers in a defence-related beta-glucosidase gene ßglu-1 with large variations in white spruce but not Norway spruce.

Conifers are long-lived and slow-evolving, thus requiring effective defences against their fast-evolving insect natural enemies. The copy number variation (CNV) of two key acetophenone biosynthesis genes Ugt5/Ugt5b and ßglu-1 may provide a plausible mechanism underlying the constitutively variable defence in white spruce (Picea glauca) against its primary defoliator, spruce budworm. This study develops a long-insert sequence capture probe set (Picea_hung_p1.0) for quantifying copy number of ßglu-1-like, Ugt5-like genes and single-copy genes on 38 Norway spruce (Picea abies) and 40 P. glauca individuals from eight and nine provenances across Europe and North America respectively. We developed local assemblies (Piabi_c1.0 and Pigla_c.1.0), full-length transcriptomes (PIAB_v1 and PIGL_v1), and gene models to characterise the diversity of ßglu-1 and Ugt5 genes. We observed very large copy numbers of ßglu-1, with up to 381 copies in a single P. glauca individual. We observed among-provenance CNV of ßglu-1 in P. glauca but not P. abies. Ugt5b was predominantly single-copy in both species. This study generates critical hypotheses for testing the emergence and mechanism of extreme CNV, the dosage effect on phenotype, and the varying copy number of genes with the same pathway. We demonstrate new approaches to overcome experimental challenges in genomic research in conifer defences.

The effect of divergent and parallel selection on the genomic landscape of divergence.

While the role of selection in divergence along the speciation continuum is theoretically well understood, defining specific signatures of selection in the genomic landscape of divergence is empirically challenging. Modelling approaches can provide insight into the potential role of selection on the emergence of a heterogenous genomic landscape of divergence. Here, we extend and apply an individual-based approach that simulates the phenotypic and genotypic distributions of two populations under a variety of selection regimes, genotype-phenotype maps, modes of migration, and genotype-environment interactions. We show that genomic islands of high differentiation and genomic valleys of similarity may respectively form under divergent and parallel selection between populations. For both types of between-population selection, negative and positive frequency-dependent selection within populations generated genomic islands of higher magnitude and genomic valleys of similarity, respectively. Divergence rates decreased under strong dominance with divergent selection, as well as in models including genotype-environment interactions under parallel selection. For both divergent and parallel selection models, divergence rate was higher under an intermittent migration regime between populations, in contrast to a constant level of migration across generations, despite an equal number of total migrants. We highlight that interpreting a particular evolutionary history from an observed genomic pattern must be done cautiously, as similar patterns may be obtained from different combinations of evolutionary processes. Modelling approaches such as ours provide an opportunity to narrow the potential routes that generate the genomic patterns of specific evolutionary histories.

Candidate gene polymorphisms are linked to dispersive and migratory behaviour: Searching for a mechanism behind the "paradox of the great speciators".

The "paradox of the great speciators" has puzzled evolutionary biologists for over half a century. A great speciator requires excellent dispersal propensity to explain its occurrence on multiple islands, but reduced dispersal ability to explain its high number of subspecies. A rapid reduction in dispersal ability is often invoked to solve this apparent paradox, but a proximate mechanism has not been identified yet. Here, we explored the role of six genes linked to migration and animal personality differences (CREB1, CLOCK, ADCYAP1, NPAS2, DRD4, and SERT) in 20 South Pacific populations of silvereye (Zosterops lateralis) that range from highly sedentary to partially migratory, to determine if genetic variation is associated with dispersal propensity and migration. We detected genetic associations in three of the six genes: (i) in a partial migrant population, migrant individuals had longer microsatellite alleles at the CLOCK gene compared to resident individuals from the same population; (ii) CREB1 displayed longer average microsatellite allele lengths in recently colonized island populations (<200 years), compared to evolutionarily older populations. Bayesian broken stick regression models supported a reduction in CREB1 length with time since colonization; and (iii) like CREB1, DRD4 showed differences in polymorphisms between recent and old colonizations but a larger sample is needed to confirm. ADCYAP1, SERT, and NPAS2 were variable but that variation was not associated with dispersal propensity. The association of genetic variants at three genes with migration and dispersal ability in silvereyes provides the impetus for further exploration of genetic mechanisms underlying dispersal shifts, and the prospect of resolving a long-running evolutionary paradox through a genetic lens.

Parasite exchange and hybridisation at a wild-feral-domestic interface.

Interactions between wild, feral, and domestic animals are of economic and conservation significance. The pigeon Columba livia is a synanthropic species in a feral form, but it also includes the rare Rock Dove. Columba livia is an important player at the wild-domestic interface, acting as a carrier of avian diseases, and the feral form threatens Rock Doves with extinction via hybridisation. Despite its abundance, little is known about drivers of disease prevalence in C. livia, or how disease and hybridisation represent synergistic threats to Rock Doves. We focused on infection by the parasite Trichomonas, first collating prevalence estimates in domestic and free-living populations from relevant studies of C. livia. Second, we characterised variation in the diversity and prevalence of Trichomonas among three C. livia populations in the United Kingdom: a feral, a Rock Dove, and a feral-wild hybrid population. Across multiple continents, free-living pigeons had lower Trichomonas infection than captive conspecifics, but the effect was weak. Environmental factors which could impact Trichomonas infection status did not explain variation in infection among populations. Among the British populations, strain diversity varied, and there was lower parasite prevalence in Rock Doves than feral pigeons. Individual infection status was not explained by the available covariates, including hybrid score and site. The drivers of Trichomonas prevalence are unclear, perhaps due to idiosyncratic local-scale drivers. However, given the population-level variation in both infection prevalence and introgressive hybridisation, the potential combined effects could accelerate the extinction of the Rock Dove. Further study of the synergistic effects of multiple types of biotic interactions at the wild-feral-domestic interface is warranted, especially where vagile, globally distributed and superabundant animals are involved.

Limited domestic introgression in a final refuge of the wild pigeon.

Domesticated animals have been culturally and economically important throughout history. Many of their ancestral lineages are extinct or genetically endangered following hybridization with domesticated relatives. Consequently, they have been understudied compared to the ancestral lineages of domestic plants. The domestic pigeon Columba livia, which was pivotal in Darwin's studies, has maintained outsized cultural significance. Its role as a model organism spans the fields of behavior, genetics, and evolution. Domestic pigeons have hybridized with their progenitor, the Rock Dove, rendering the latter of dubious genetic status. Here, we use genomic and morphological data from the putative Rock Doves of the British Isles to identify relictual undomesticated populations. We reveal that Outer Hebridean Rock Doves have experienced minimal levels of introgression. Our results outline the contemporary status of these wild pigeons, highlighting the role of hybridization in the homogenization of genetic lineages.

The wild ancestors of domestic animals as a neglected and threatened component of biodiversity.

Domestic animals have immense economic, cultural, and practical value and have played pivotal roles in the development of human civilization. Many domesticates have, among their wild relatives, undomesticated forms representative of their ancestors. Resurgent interest in these ancestral forms has highlighted the unclear genetic status of many, and some are threatened with extinction by hybridization with domestic conspecifics. We considered the contemporary status of these ancestral forms relative to their scientific, practical, and ecological importance; the varied impacts of wild-domestic hybridization; and the challenges and potential resolutions involved in conservation efforts. Identifying and conserving ancestral forms, particularly with respect to disentangling patterns of gene flow from domesticates, is complex because of the lack of available genomic and phenotypic baselines. Comparative behavioral, ecological, and genetic studies of ancestral-type, feral, and domestic animals should be prioritized to establish the contemporary status of the former. Such baseline information will be fundamental in ensuring successful conservation efforts.

Los Ancestros de Animales Domésticos como un Componente Descuidado y Amenazado de la Biodiversidad Resumen Los animales domésticos tienen un inmenso valor económico, cultural y práctico y han jugado un papel muy importante en el desarrollo de la civilización humana. Muchos animales domesticados tienen, entre sus parientes silvestres, formas no domesticadas representativas de sus ancestros. Un interés renovado en estas formas ancestarles ha destacado el estatus genético poco claro de muchas, y algunas están amenazadas de extinción por hibridación con conespecíficos domesticados. Consideramos el estatus contempóraneo de estas formas ancestrales en relación con su importancia científica, práctica y ecológica; los impactos diversos de la hibridación silvestre-domesticado; y los retos y soluciones potenciales involucrados en los esfuerzos de conservación. La identificación y conservación de formas ancestrales, particularmente en relación con desenredar patrones de flujo génicos, es compleja debido a la carencia de líneas de base genómicas y fenotípicas. Se deben priorizar estudios conductuales, ecológicos y genéticos comparativos de los animales ancestrales, ferales y domésticos para establecer el estatus contemporáno de los primeros. Tal información de base será fundamental para asegurar esfuerzos de conservación exitosos.

An island-hopping bird reveals how founder events shape genome-wide divergence.

When populations colonize new areas, both strong selection and strong drift can be experienced due to novel environments and small founding populations, respectively. Empirical studies have predominantly focused on the phenotype when assessing the role of selection, and limited neutral-loci when assessing founder-induced loss of diversity. Consequently, the extent to which processes interact to influence evolutionary trajectories is difficult to assess. Genomic-level approaches provide the opportunity to simultaneously consider these processes. Here, we examine the roles of selection and drift in shaping genomic diversity and divergence in historically documented sequential island colonizations by the silvereye (Zosterops lateralis). We provide the first empirical demonstration of the rapid appearance of highly diverged genomic regions following population founding, the position of which are highly idiosyncratic. As these regions rarely contained loci putatively under selection, it is most likely that these differences arise via the stochastic nature of the founding process. However, selection is required to explain rapid evolution of larger body size in insular silvereyes. Reconciling our genomic data with these phenotypic patterns suggests there may be many genomic routes to the island phenotype, which vary across populations. Finally, we show that accelerated divergence associated with multiple founding steps is the product of genome-wide rather than localized differences, and that diversity erodes due to loss of rare alleles. However, even multiple founder events do not result in divergence and diversity levels seen in evolutionary older subspecies, and therefore do not provide a shortcut to speciation as proposed by founder-effect speciation models.

The Genomic Landscape of Divergence Across the Speciation Continuum in Island-Colonising Silvereyes (Zosterops lateralis).

Inferring the evolutionary dynamics at play during the process of speciation by analyzing the genomic landscape of divergence is a major pursuit in population genomics. However, empirical assessments of genomic landscapes under varying evolutionary scenarios that are known a priori are few, thereby limiting our ability to achieve this goal. Here we combine RAD-sequencing and individual-based simulations to evaluate the genomic landscape of divergence in the silvereye (Zosterops lateralis). Using pairwise comparisons that differ in divergence timeframe and the presence or absence of gene flow, we document how genomic patterns accumulate along the speciation continuum. In contrast to previous predictions, our results provide limited support for the idea that divergence accumulates around loci under divergent selection or that genomic islands widen with time. While a small number of genomic islands were found in populations diverging with and without gene flow, in few cases were SNPs putatively under selection tightly associated with genomic islands. The transition from localized to genome-wide levels of divergence was captured using individual-based simulations that considered only neutral processes. Our results challenge the ubiquity of existing verbal models that explain the accumulation of genomic differences across the speciation continuum and instead support the idea that divergence both within and outside of genomic islands is important during the speciation process.

Life-history strategy varies with the strength of competition in a food-limited ungulate population.

Fluctuating population density in stochastic environments can contribute to maintain life-history variation within populations via density-dependent selection. We used individual-based data from a population of Soay sheep to examine variation in life-history strategies at high and low population density. We incorporated life-history trade-offs among survival, reproduction and body mass growth into structured population models and found support for the prediction that different life-history strategies are optimal at low and high population densities. Shorter generation times and lower asymptotic body mass were selected for in high-density environments even though heavier individuals had higher probabilities to survive and reproduce. In contrast, greater asymptotic body mass and longer generation times were optimal at low population density. If populations fluctuate between high density when resources are scarce, and low densities when they are abundant, the variation in density will generate fluctuating selection for different life-history strategies, that could act to maintain life-history variation.

Rapid morphological divergence following a human-mediated introduction: the role of drift and directional selection.

Theory predicts that when populations are established by few individuals, random founder effects can facilitate rapid phenotypic divergence even in the absence of selective processes. However, empirical evidence from historically documented colonisations suggest that, in most cases, drift alone is not sufficient to explain the rate of morphological divergence. Here, using the human-mediated introduction of the silvereye (Zosterops lateralis) to French Polynesia, which represents a potentially extreme example of population founding, we reassess the potential for morphological shifts to arise via drift alone. Despite only 80 years of separation from their New Zealand ancestors, French Polynesian silvereyes displayed significant changes in body and bill size and shape, most of which could be accounted for by drift, without the need to invoke selection. However, signatures of selection at genes previously identified as candidates for bill size and body shape differences in a range of bird species, also suggests a role for selective processes in driving morphological shifts within this population. Twenty-four SNPs in our RAD-Seq dataset were also found to be strongly associated with phenotypic variation. Hence, even under population founding extremes, when it is difficult to reject drift as the sole mechanism based on rate tests of phenotypic shifts, the additional role of divergent natural selection in novel environments can be revealed at the level of the genome.

A simple dynamic model explains the diversity of island birds worldwide.

Colonization, speciation and extinction are dynamic processes that influence global patterns of species richness1-6. Island biogeography theory predicts that the contribution of these processes to the accumulation of species diversity depends on the area and isolation of the island7,8. Notably, there has been no robust global test of this prediction for islands where speciation cannot be ignored9, because neither the appropriate data nor the analytical tools have been available. Here we address both deficiencies to reveal, for island birds, the empirical shape of the general relationships that determine how colonization, extinction and speciation rates co-vary with the area and isolation of islands. We compiled a global molecular phylogenetic dataset of birds on islands, based on the terrestrial avifaunas of 41 oceanic archipelagos worldwide (including 596 avian taxa), and applied a new analysis method to estimate the sensitivity of island-specific rates of colonization, speciation and extinction to island features (area and isolation). Our model predicts-with high explanatory power-several global relationships. We found a decline in colonization with isolation, a decline in extinction with area and an increase in speciation with area and isolation. Combining the theoretical foundations of island biogeography7,8 with the temporal information contained in molecular phylogenies10 proves a powerful approach to reveal the fundamental relationships that govern variation in biodiversity across the planet.

The effect of insularity on avian growth rates and implications for insular body size evolution.

Island populations often differ in consistent ways from their mainland counterparts with respect to their ecology, behaviour, morphology, demography and life-history characteristics; a set of changes referred to as the 'island syndrome'. To understand the ecological and evolutionary drivers of the island syndrome requires characterization of suites of interacting traits. While patterns in some types of traits, e.g. body size, are well characterized across a range of taxa, key gaps remain. Growth rate is one such trait, being an important determinant of both increases and decreases in body size, and can vary with changes in predation pressure and food limitation; two factors that are known to differ between mainland and island environments. Using a phylogenetic meta-analytic approach, we characterize differences in growth rates among mainland and island altricial bird populations, controlling for environmental factors. We found a trend towards slower growth on islands in small-bodied (less than 1 kg) bird species. This is consistent with the idea that the pattern of body size increases in small-bodied island colonists is associated with the evolution of slower growth combined with shifts in age and size at maturity in relaxed predation regimes.

Climate variation influences host specificity in avian malaria parasites.

Parasites with low host specificity (e.g. infecting a large diversity of host species) are of special interest in disease ecology, as they are likely more capable of circumventing ecological or evolutionary barriers to infect new hosts than are specialist parasites. Yet for many parasites, host specificity is not fixed and can vary in response to environmental conditions. Using data on host associations for avian malaria parasites (Apicomplexa: Haemosporida), we develop a hierarchical model that quantifies this environmental dependency by partitioning host specificity variation into region- and parasite-level effects. Parasites were generally phylogenetic host specialists, infecting phylogenetically clustered subsets of available avian hosts. However, the magnitude of this specialisation varied biogeographically, with parasites exhibiting higher host specificity in regions with more pronounced rainfall seasonality and wetter dry seasons. Recognising the environmental dependency of parasite specialisation can provide useful leverage for improving predictions of infection risk in response to global climate change.

Response to Comment on "Precipitation drives global variation in natural selection".

The comment by Myers-Smith and Myers focuses on three main points: (i) the lack of a mechanistic explanation for climate-selection relationships, (ii) the appropriateness of the climate data used in our analysis, and (iii) our focus on estimating climate-selection relationships across (rather than within) taxonomic groups. We address these critiques in our response.

The influence of climatic variation and density on the survival of an insular passerine Zosterops lateralis.

Understanding the influence of environmental factors on population dynamics is fundamental to many areas in biology. Survival is a key factor of population biology, as it is thought to be the predominant driver of growth in long-lived passerines, which can be influenced by both biotic and abiotic environmental conditions. We used mark-recapture methods and generalized linear mixed models to test the influence of density and climatic variation, measured at a regional and local scale (Southern Oscillation Index [SOI] and rainfall, respectively), on seasonal variation in survival rates of an insular population of Silvereyes (Zosterops lateralis chlorocephalus), during a 15-year study period, off the east coast of Australia. We found overall high survival rates for adults and juveniles (81% and 59%, respectively). Local scale climate (i.e. rainfall) and density were the principal environmental factors influencing their survival, both with a negative relationship. A significant interactive effect of density and rainfall influenced survival as they both increased. However, survival remained low when density was at it highest, independent of the amount of rainfall. Nestling survival was negatively influenced by rainfall and density, positively by SOI, and chicks that hatched later in the breeding season had higher survival rates. The regional scale climate variable (i.e. SOI) did not explain survival rates as strongly as rainfall in any age class. Our results contribute to the understanding of insular avian population dynamics and the differential effects of environmental factors across age classes. Climatic predictions expect El Niño events to increase, meaning dryer conditions in eastern Australia, potentially increasing Silvereye survival across age classes. However, the long-term effect of lower rainfall on food availability is unknown; consequently, the outcome of lower rainfall on Silvereye survival rates is uncertain.

Integrating phylogenetic and ecological distances reveals new insights into parasite host specificity.

The range of hosts a pathogen infects (host specificity) is a key element of disease risk that may be influenced by both shared phylogenetic history and shared ecological attributes of prospective hosts. Phylospecificity indices quantify host specificity in terms of host relatedness, but can fail to capture ecological attributes that increase susceptibility. For instance, similarity in habitat niche may expose phylogenetically unrelated host species to similar pathogen assemblages. Using a recently proposed method that integrates multiple distances, we assess the relative contributions of host phylogenetic and functional distances to pathogen host specificity (functional-phylogenetic host specificity). We apply this index to a data set of avian malaria parasite (Plasmodium and Haemoproteus spp.) infections from Melanesian birds to show that multihost parasites generally use hosts that are closely related, not hosts with similar habitat niches. We also show that host community phylogenetic ß-diversity (Pßd) predicts parasite Pßd and that individual host species carry phylogenetically clustered Haemoproteus parasite assemblages. Our findings were robust to phylogenetic uncertainty, and suggest that phylogenetic ancestry of both hosts and parasites plays important roles in driving avian malaria host specificity and community assembly. However, restricting host specificity analyses to either recent or historical timescales identified notable exceptions, including a 'habitat specialist' parasite that infects a diversity of unrelated host species with similar habitat niches. This work highlights that integrating ecological and phylogenetic distances provides a powerful approach to better understand drivers of pathogen host specificity and community assembly.

Precipitation drives global variation in natural selection.

Climate change has the potential to affect the ecology and evolution of every species on Earth. Although the ecological consequences of climate change are increasingly well documented, the effects of climate on the key evolutionary process driving adaptation-natural selection-are largely unknown. We report that aspects of precipitation and potential evapotranspiration, along with the North Atlantic Oscillation, predicted variation in selection across plant and animal populations throughout many terrestrial biomes, whereas temperature explained little variation. By showing that selection was influenced by climate variation, our results indicate that climate change may cause widespread alterations in selection regimes, potentially shifting evolutionary trajectories at a global scale.

Co-infections and environmental conditions drive the distributions of blood parasites in wild birds.

Experimental work increasingly suggests that non-random pathogen associations can affect the spread or severity of disease. Yet due to difficulties distinguishing and interpreting co-infections, evidence for the presence and directionality of pathogen co-occurrences in wildlife is rudimentary. We provide empirical evidence for pathogen co-occurrences by analysing infection matrices for avian malaria (Haemoproteus and Plasmodium spp.) and parasitic filarial nematodes (microfilariae) in wild birds (New Caledonian Zosterops spp.). Using visual and genus-specific molecular parasite screening, we identified high levels of co-infections that would have been missed using PCR alone. Avian malaria lineages were assigned to species level using morphological descriptions. We estimated parasite co-occurrence probabilities, while accounting for environmental predictors, in a hierarchical multivariate logistic regression. Co-infections occurred in 36% of infected birds. We identified both positively and negatively correlated parasite co-occurrence probabilities when accounting for host, habitat and island effects. Two of three pairwise avian malaria co-occurrences were strongly negative, despite each malaria parasite occurring across all islands and habitats. Birds with microfilariae had elevated heterophil to lymphocyte ratios and were all co-infected with avian malaria, consistent with evidence that host immune modulation by parasitic nematodes facilitates malaria co-infections. Importantly, co-occurrence patterns with microfilariae varied in direction among avian malaria species; two malaria parasites correlated positively but a third correlated negatively with microfilariae. We show that wildlife co-infections are frequent, possibly affecting infection rates through competition or facilitation. We argue that combining multiple diagnostic screening methods with multivariate logistic regression offers a platform to disentangle impacts of environmental factors and parasite co-occurrences on wildlife disease.