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The “paradox of the great speciators” has puzzled evolutionary biologists for over half a century. A great speciator requires excellent dispersal ability 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. Here, we explore the role of six genes linked to migration and animal personality differences (CREB1, CLOCK, ADCYAP1, NPAS2, DRD4, andSERT) 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. We detected genetic associations in three of the six genes: i) in a partial migrant population, migrant individuals had longer microsatellite alleles at theCLOCKgene compared to resident individuals from the same population; ii)CREB1displayed longer average microsatellite allele lengths in recently colonised island populations (< 200 years), compared to evolutionarily older populations. Bayesian broken stick regression models supported a reduction inCREB1length with time since colonisation and decreasing dispersal propensity; and iii) likeCREB1, DRD4showed differences in polymorphisms between recent and old colonisations but a further sample size is needed to confirm.ADCYAP1, SERT, andNPAS2were 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.

A fundamental goal in evolutionary biology is to understand the genetic architecture of adaptive traits and its evolutionary relevance. Using whole-genome data of 3,958 Darwin’s finches on the Galápagos Island of Daphne Major we identify six loci of large effect that explain 46% of the variation in beak size ofGeospiza fortis, a key ecological trait. Allele frequency changes across 30 years at these loci affected beak morphology in two ways. An abrupt change in beak size occurred inGeospiza fortisas a result of natural selection associated with a drought, and a more gradual change occurred inG. scandensas a result of introgressive hybridization. This study demonstrates how large effect loci are a major contributor to the genetic architecture of rapid diversification during adaptive radiations.One Sentence SummaryAllele frequency change at six loci of large effect causes evolutionary change in key ecological traits.

Recent adaptive radiations are models for investigating mechanisms contributing to the evolution of biodiversity. An unresolved question is the relative importance of new mutations, ancestral variants, and introgressive hybridization for phenotypic evolution and speciation. Here, we address this issue using Darwin's finches and investigate the genomic architecture underlying their phenotypic diversity. Admixture mapping for beak and body size in the small, medium, and large ground finches revealed 28 loci showing strong genetic differentiation. These loci represent ancestral haplotype blocks with origins predating speciation events during the Darwin's finch radiation. Genes expressed in the developing beak are overrepresented in these genomic regions. Ancestral haplotypes constitute genetic modules for selection and act as key determinants of the unusual phenotypic diversity of Darwin's finches. Such ancestral haplotype blocks can be critical for how species adapt to environmental variability and change.

A goal of the genomic era is to infer the evolutionary dynamics at play during the process of speciation by analysing the genomic landscape of divergence. However, empirical assessments of genomic landscapes under varying evolutionary scenarios are few, limiting the ability to achieve this goal. Here we combine RAD-sequencing and individual-based simulations to evaluate the genomic landscape in the silvereye (Zosterops lateralis). Using comparisons matched for divergence timeframe and gene flow context, 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. Furthermore, we modelled the transition from localised to genome-wide levels of divergence 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.DATA ACCESSION NUMBERSResequencing data from this study have been submitted to the National Center for Biotechnology Information (NCBI; https://www.ncbi.nlm.nih.gov) under accession number PRJNA489169.

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.【摘要】家畜具有巨大的经济、文化和实用价值, 在人类文明的发展中发挥了关键作用。许多家畜的野生近缘物种中都有代表其祖先型的未驯化动物。重新关注这些祖先型的动物, 会发现其中许多的遗传状态不明确, 还有些因为与同种的家畜发生杂交而面临灭绝的威胁。我们分析了这些祖先型动物目前在科学、实用和生态方面的重要性、野生动物与家畜杂交的各种影响, 以及保护工作中的挑战和潜在的解决方案。由于缺乏可用的基因组和表型基线数据, 识别和保护祖先型动物仍是十分复杂的问题, 特别是解析其受到来自家畜的基因流模式。我们建议应优先考虑对祖先型动物、野生动物和家畜的行为学、生态学和遗传学进行比较研究, 以确定前者当前的状态。这些基线信息是确保保护工作成功的基础。【翻译: 胡怡思; 审校: 聂永刚】.

Domesticated animals have been culturally and economically important throughout history. Many of their ancestral lineages are extinct or genetically en dangered 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 sta tus. 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 introgres sion. Our results outline the contemporary status of these wild pigeons, high lighting the role of hybridization in the homogenization of genetic lineages.

When populations colonise 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 colonisations by the silvereye bird (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, that vary across populations. Finally, we show that accelerated divergence associated with multiple founding steps is the product of genome-wide rather than localised 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.

Can divergence in a mating trait increase local adaption by increasing ecological divergence? Servedio and Bürger propose that "pseudomagic traits," tightly linked complexes consisting of an ecological locus under divergent selection and a locus acting as a mating cue, can effectively mimic pleiotropy. Such pseudomagic traits can form even when linkage between ecological and mating loci is limited.

Speciation is a dynamic process, shaped by interactions among different evolutionary mechanisms including natural selection, genetic drift, gene flow, and mutation. Over 150 years since the publication of ‘On the Origin of Species’ a major challenge in evolutionary biology is to determine the relative importance of these different mechanisms in the speciation process. In the era of genomics, a step towards addressing this challenge is to study the progression of speciation at the level of the genome. Using island colonisations by the silvereye (Zosterops lateralis), in this thesis I investigate the roles of gene flow, selection and drift in shaping patterns of divergence at both the genomic and phenotypic level. In Chapter 2, using populations where divergence timeframes and gene flow histories are known a priori, I documented how genomic patterns accumulate as populations progress along the speciation continuum. This chapter challenges the ubiquity of existing verbal models that explain the accumulation of genomic differences via the growth of genomic islands and instead supports the idea that divergence both within and outside of genomic islands is important during the speciation process. In Chapter 3, using the recent sequential colonization of south Pacific islands by the Tasmanian silvereye subspecies I provide the first assessment of how patterns of genomic divergence are shaped by the stochastic effects of drift following population founding. By tracking divergence across the genome, I demonstrate that population founding has an idiosyncratic effect on the buildup of divergence. In Chapter 4, using the human- mediated introduction of the silvereye to French Polynesia, I assess the role of drift and selection in driving rapid morphological change following the establishment of new populations. Despite only 80 years of separation from their New Zealand ancestors, French Polynesian silvereyes displayed significant changes in body and bill size and shape, but the magnitude of these changes are not large enough, considering effective population sizes, to require directional natural selection to explain them; instead drift alone is a sufficient explanation at the phenotypic level. However, identification of outlier loci at genes previously identified as candidates for bill size and body shape, also suggests selective processes are operating within this population. As a whole, this body of work furthers understanding of how different evolutionary mechanisms shape patterns of divergence at the level of the genome and how divergence unfolds following the establishment of new populations.

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.

1. The way that organisms diverge into reproductively isolated species is a major question in biology. The recent accumulation of genomic data provides promising opportunities to understand the genomic landscape of divergence, which describes the distribution of differences across genomes. Genomic areas of unusually high differentiation have been called genomic islands of divergence. Their formation has been attributed to a variety of mechanisms, but a prominent hypothesis is that they result from divergent selection over a small portion of the genome, with surrounding areas homogenised by gene flow. Such islands have often been interpreted as being associated with divergence with gene flow. However other mechanisms related to genetic architecture and population history can also contribute to the formation of genomic islands of divergence.2. We currently lack a quantitative framework to examine the dynamics of genomic landscapes under the complex and nuanced conditions that are found in natural systems. Here, we develop an individual-based simulation to explore the dynamics of diverging genomes under various scenarios of gene flow, selection and genotype-phenotype maps.3. Our modelling results are consistent with empirical observations demonstrating the formation of genomic islands under genetic isolation. Importantly, we have quantified the range of conditions that produce genomic islands. We demonstrate that the initial level of genetic diversity, drift, time since divergence, linkage disequilibrium, strength of selection and gene flow are all important factors that can influence the formation of genomic islands. Because the accumulation of genomic differentiation over time tends to erode the signal of genomic islands, genomic islands are more likely to be observed in recently divergent taxa, although not all recently diverged taxa will necessarily exhibit islands of genomic divergence. Gene flow primarily slows the swamping of islands of divergence with time.4. By using this framework, further studies may explore the relative influence of particular suites of events that contribute to the emergence of genomic islands under sympatric, parapatric and allopatric conditions. This approach represents a novel tool to explore quantitative expectations of the speciation process, and should prove useful in elucidating past and projecting future genomic evolution of any taxa.