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The concept of a “speciation continuum” has gained popularity in recent decades. It emphasizes speciation as a continuous process that may be studied by comparing contemporary population pairs that show differing levels of divergence. In their recent perspective article in Evolution, Stankowski and Ravinet provided a valuable service by formally defining the speciation continuum as a continuum of reproductive isolation, based on opinions gathered from a survey of speciation researchers. While we agree that the speciation continuum has been a useful concept to advance the understanding of the speciation process, some intrinsic limitations exist. Here, we advocate for a multivariate extension, the speciation hypercube, first proposed by Dieckmann et al. in 2004, but rarely used since. We extend the idea of the speciation cube and suggest it has strong conceptual and practical advantages over a one-dimensional model. We illustrate how the speciation hypercube can be used to visualize and compare different speciation trajectories, providing new insights into the processes and mechanisms of speciation. A key strength of the speciation hypercube is that it provides a unifying framework for speciation research, as it allows questions from apparently disparate subfields to be addressed in a single conceptual model.

Range expansion is a common natural phenomenon, which may be intensified by human-induced drivers such as climate change and alterations of habitat. The genetic consequences of range expansion are potentially major, and it is important to study known cases of range expansion to understand how human activities affect contemporary evolution, and to learn more about the genetic adaptive potential of species. The reed warbler (Acrocephalus scirpaceus) is a long-distance migratory bird breeding in Eurasia and wintering south of Sahara. It is currently expanding its range northwards, likely as a consequence of climate change. Interestingly, however, reed warblers have also recently colonised new territory southwards, following habitat restoration at the southern range margin. In this study, we investigate the genetic consequences of these two-directional range expansions with RAD-seq, looking at 10 populations from north to south in Europe. We investigate population structure and genome diversity, and assess the role of selection in divergence between populations across the species range. We do not find evidence of strong genetic structure in the reed warbler populations, and the youngest edge populations do not exhibit any substantial loss in genetic diversity, suggesting ongoing gene flow. On a smaller scale, the edge populations are the most genetically distinct, and we identify environmental disparity, especially in precipitation variability, as the main barrier of gene flow, to a greater extent than geographic distance. We find no evidence that the loci involved in population divergence and adaptation in the core populations are the same that are involved in adaptation at the range edges. Using three genome scan methods to identify selection, we found 49 SNPs putatively under selection, of which 33 were located in introns of 28 unique genes. Most of these are correlated with differences in climatic variables of temperature and precipitation. Some genome scan outliers show signs of being part of nascent selective sweeps, especially one which is distinct for the northern range edge. Our results suggest that in the reed warbler, contemporary range expansion has had little effect on molecular diversity and has been rapidly followed by local adaptation to climatic conditions, which could further corroborate the rapid pace at which colonisation of novel environments has occurred both northwards and southwards.

To understand how species evolve and adapt to changing environments, it is important to study gene flow and introgression due to their influence on speciation and radiation events. Here, we apply a novel experimental system for investigating these mechanisms using natural populations. The system is based on two fungal sister species with morphological and ecological similarities occurring in overlapping habitats. We examined introgression between these species by conducting whole genome sequencing of individuals from populations in North America and Europe. We assessed genome wide nucleotide divergence and performed crossing experiments to study reproductive barriers. We further used ABBA-BABA statistics together with a network analysis to investigate introgression, and conducted demographic modelling to gain insight into divergence times and introgression events. The results revealed that the species are highly divergent and incompatible in vitro. Despite this, small regions of introgression were scattered throughout the genomes and one introgression event likely involves a ghost population (extant or extinct). This study demonstrates that introgression can be found among divergent species and that population histories can be studied without collections of all the populations involved. Moreover, the experimental system is shown to be a useful tool for research on reproductive isolation in natural populations.

Chromosomal inversions have been shown to play a major role in a local adaptation by suppressing recombination between alternative arrangements and maintaining beneficial allele combinations. However, so far, their importance relative to the remaining genome remains largely unknown. Understanding the genetic architecture of adaptation requires better estimates of how loci of different effect sizes contribute to phenotypic variation. Here, we used three Swedish islands where the marine snail Littorina saxatilis has repeatedly evolved into two distinct ecotypes along a habitat transition. We estimated the contribution of inversion polymorphisms to phenotypic divergence while controlling for polygenic effects in the remaining genome using a quantitative genetics framework. We confirmed the importance of inversions but showed that contributions of loci outside inversions are of similar magnitude, with variable proportions dependent on the trait and the population. Some inversions showed consistent effects across all sites, whereas others exhibited site-specific effects, indicating that the genomic basis for replicated phenotypic divergence is only partly shared. The contributions of sexual dimorphism as well as environmental factors to phenotypic variation were significant but minor compared to inversions and polygenic background. Overall, this integrated approach provides insight into the multiple mechanisms contributing to parallel phenotypic divergence.

Does evolution proceed in small steps or large leaps? How repeatable is evolution? How constrained is the evolutionary process? Answering these long-standing questions in evolutionary biology is indispensable for both understanding how extant biodiversity has evolved and predicting how organisms and ecosystems will respond to changing environments in the future. Understanding the genetic basis of phenotypic diversification and speciation in natural populations is key to properly answering these questions. The leap forward in genome sequencing technologies has made it increasingly easier to not only investigate the genetic architecture but also identify the variant sites underlying adaptation and speciation in natural populations. Furthermore, recent advances in genome editing technologies are making it possible to investigate the functions of each candidate gene in organisms from natural populations. In this article, we discuss how these recent technological advances enable the analysis of causative genes and mutations and how such analysis can help answer long-standing evolutionary biology questions. This article is part of the theme issue ‘Genetic basis of adaptation and speciation: from loci to causative mutations’.

With only a few absolute geographic barriers in marine environments, the factors maintaining reproductive isolation among marine organisms remain elusive. However, spatial structuring in breeding habitat can contribute to reproductive isolation. This is particularly important for marine organisms that migrate to use fresh- or brackish water environments to breed. The Japanese Gasterosteus stickleback species, the Pacific Ocean three-spined stickleback (G. aculeatus) and the Japan Sea stickleback (G. nipponicus) overwinter in the sea, but migrate to rivers for spawning. Although they co-occur at several locations across the Japanese islands, they are reproductively isolated. Our previous studies in Bekanbeushi River showed that the Japan Sea stickleback spawns in the estuary, while the Pacific Ocean stickleback mainly spawns further upstream in freshwater. Overall genomic divergence was very high with many interspersed regions of introgression. Here, we investigated genomic divergence and introgression between the sympatric species in the much shorter Tokotan River, where they share spawning sites. The levels of genome-wide divergence were reduced and introgression was increased, suggesting that habitat isolation substantially contributes to a reduction in gene flow. We also found that genomic regions of introgression were largely shared between the two systems. Furthermore, some regions of introgression were located near loci with a heterozygote advantage for juvenile survival. Taken together, introgression may be partially driven by adaptation in this system. Although, the two species remain clearly genetically differentiated. Regions with low recombination rates showed especially low introgression. Speciation reversal is therefore likely prevented by barriers other than habitat isolation.

Hybridization can result in novel allelic combinations which can impact the hybrid phenotype through changes in gene expression. While mis-expression in F1 hybrids is well documented, how gene expression evolves in stabilized hybrid taxa remains an open question. As gene expression evolves in a stabilizing manner, break-up of co-evolved cis- and trans-regulatory elements could lead to transgressive patterns of gene expression in hybrids. Here, we address to what extent gonad gene expression has evolved in an established and stable homoploid hybrid, the Italian sparrow (Passer italiae). Through comparison of gene expression in gonads from individuals of the two parental species (i.e., house and Spanish sparrow) to that of Italian sparrows, we find evidence for strongly transgressive expression in male Italian sparrows - 22% of testis genes exhibit expression patterns outside the range of both parent species. In contrast, Italian sparrow ovary expression was similar to that of one of the parent species, the house sparrow (Passer domesticus). Moreover, the Italian sparrow testis transcriptome is 26 times as diverged from those of the parent species as the parental transcriptomes are from each other, despite being genetically intermediate. This highlights the potential for regulation of gene expression to produce novel variation following hybridization. Genes involved in mitochondrial respiratory chain complexes and protein synthesis are enriched in the subset that is over-dominantly expressed in Italian sparrow testis, suggesting that selection on key functions have molded the hybrid Italian sparrow transcriptome.

Adaptive radiations have proven important for understanding the mechanisms and processes underlying biological diversity. The convergence of form and function, as well as admixture and adaptive introgression, are common in adaptive radiations. However, distinguishing between these two scenarios remains a challenge for evo-lutionary research. The Midas cichlid species complex (Amphilophus spp.) is a prime example of adaptive radiation, with phenotypic diversification occurring at various stages of genetic differentiation. One species, A. labiatus, has large fleshy lips, is as-sociated with rocky lake substrates, and occurs patchily within Lakes Nicaragua and Managua. By contrast, the similar, but thin- lipped, congener, A. citrinellus, is more com-mon and widespread. We investigated the evolutionary history of the large- lipped form, specifically regarding whether the trait has evolved independently in both lakes from ancestral thin- lipped populations, or via dispersal and/or admixture events. We collected samples from distinct locations in both lakes, and assessed differences in morphology and ecology. Using RAD-seq, we genotyped thousands of SNPs to measure population structure and divergence, demographic history, and admixture. We found significant between-species differences in ecology and morphology, local intraspecific differences in body shape and trophic traits, but only limited intraspe-cific variation in lip shape. Despite clear ecological differences, our genomic approach uncovered pervasive admixture between the species and low genomic differentiation, with species within lakes being genetically more similar than species between lakes. Taken together, our results suggest a single origin of large-lips, followed by pervasive admixture and adaptive introgression, with morphology being driven by local ecologi-cal opportunities, despite ongoing gene-flow., Funding was also provided by a Monash University travel grant (to WS) and from the SYNTHESYS Project (http://www.synthesys.info/) financed by the European Community Research Infrastructure Action under the FP7 "Capacities" Program (to TKL and MB).

Both classical and recent studies suggest that chromosomal inversion polymorphisms are important in adaptation and speciation. However, biases in discovery and reporting of inversions make it difficult to assess their prevalence and biological importance. Here, we use an approach based on linkage disequilibrium among markers genotyped for samples collected across a transect between contrasting habitats to detect chromosomal rearrangements de novo. We report 17 polymorphic rearrangements in a single locality for the coastal marine snail, Littorina saxatilis. Patterns of diversity in the field and of recombination in controlled crosses provide strong evidence that at least the majority of these rearrangements are inversions. Most show clinal changes in frequency between habitats, suggestive of divergent selection, but only one appears to be fixed for different arrangements in the two habitats. Consistent with widespread evidence for balancing selection on inversion polymorphisms, we argue that a combination of heterosis and divergent selection can explain the observed patterns and should be considered in other systems spanning environmental gradients. This article is protected by copyright. All rights reserved.

Humans conceptualize the diversity of life by classifying individuals into types we call 'species'1. The species we recognize influence political and financial decisions and guide our understanding of how units of diversity evolve and interact. Although the idea of species may seem intuitive, a debate about the best way to define them has raged even before Darwin2. So much energy has been devoted to the so-called 'species problem' that no amount of discourse will ever likely solve it2,3. Dozens of species concepts are currently recognized3, but we lack a concrete understanding of how much researchers actually disagree and the factors that cause them to think differently1,2. To address this, we used a survey to quantify the species problem for the first time. The results indicate that the disagreement is extensive: two randomly chosen respondents will most likely disagree on the nature of species. The probability of disagreement is not predicted by researcher experience or broad study system, but tended to be lower among researchers with similar focus, training and who study the same organism. Should we see this diversity of perspectives as a problem? We argue that we should not.

Pathogens may elicit a high selective pressure on hosts and can alter genetic diversity over short evolutionary timescales. Intraspecific variation in immune response can be observed as variable survivability from specific infections. The great gerbil (Rhombomys opimus) is a rodent plague host with a heterogenic but highly resistant phenotype. Here, we investigate if the most plague-resistant phenotypes are linked to genomic differences between survivors and susceptible individuals by exposure of wild-caught great gerbils from Northwest China to plague (Yersinia pestis). Whole genome sequencing of ten survivors and ten moribund individuals revealed a low genome-wide mean divergence, except for a subset of genomic regions that showed elevated differentiation. Gene ontology (GO) analysis of candidate genes within regions of increased differentiation, demonstrated enrichment of pathways involved in transcription and translation and their regulation), as well as genes directly involved in immune functions, cellular metabolism and the regulation of apoptosis. Differential RNA expression analysis revealed that the early activated great gerbil immune response to plague consisted of classical components of the innate immune system. Our approach combining challenge experiments with transcriptomics and population level sequencing, provides new insight into the genetic background of plague-resistance and confirms its complex nature, most likely involving multiple genes and pathways of both the immune system and regulation of basic cellular functions.

Hybridization is increasingly recognized as an important evolutionary force. Novel genetic methods now enable us to address how the genomes of parental species are combined to build hybrid genomes. However, we still do not know the relative importance of contingencies, genome architecture and local selection in shaping hybrid genomes. Here, we take advantage of the genetically divergent island populations of Italian sparrow on Crete, Corsica and Sicily to investigate the predictors of genomic variation within a hybrid taxon. We test if differentiation is affected by recombination rate, selection, or variation in ancestry proportion from each parent species. We find that the relationship between recombination rate and differentiation is less pronounced within hybrid lineages than between the parent species, as expected if purging of minor parent ancestry in low recombination regions reduces the variation available for differentiation. In addition, we find that differentiation between islands is correlated with differences in selection in two out of three comparisons. Patterns of within-island selection are correlated across all islands, suggesting that shared selection may mould genomic differentiation. The best predictor of strong differentiation within islands is the degree of differentiation from house sparrow, and hence loci with Spanish sparrow ancestry may vary more freely. Jointly, this suggests that constraints and selection interact in shaping the genomic landscape of differentiation in this hybrid species.

A primary roadblock to our understanding of speciation is that it usually occurs over a timeframe that is too long to study from start to finish. The idea of a speciation continuum provides something of a solution to this problem; rather than observing the entire process, we can simply reconstruct it from the multitude of speciation events that surround us. But what do we really mean when we talk about the speciation continuum, and can it really help us understand speciation? We explored these questions using a literature review and online survey of speciation researchers. Although most researchers were familiar with the concept and thought it was useful, our survey revealed extensive disagreement about what the speciation continuum actually tells us. This is due partly to the lack of a clear definition. Here, we provide an explicit definition that is compatible with the Biological Species Concept. That is, the speciation continuum is a continuum of reproductive isolation. After outlining the logic of the definition in light of alternatives, we explain why attempts to reconstruct the speciation process from present-day populations will ultimately fail. We then outline how we think the speciation continuum concept can continue to act as a foundation for understanding the continuum of reproductive isolation that surrounds us. This article is protected by copyright. All rights reserved.

Morphologically similar species, that is cryptic species, may be similar or quasi-similar owing to the deceleration of morphological evolution and stasis. While the factors underlying the deceleration of morphological evolution or stasis in cryptic species remain unknown, decades of research in the field of paleontology on punctuated equilibrium have originated clear hypotheses. Species are expected to remain morphologically identical in scenarios of shared genetic variation, such as hybridization and incomplete lineage sorting, or in scenarios where bottlenecks reduce genetic variation and constrain the evolution of morphology. Here, focusing on three morphologically similar Stygocapitella species, we employ a whole-genome amplification method (WGA) coupled with double-digestion restriction-site associated DNA sequencing (ddRAD) to reconstruct the evolutionary history of the species complex. We explore population structure, use population-level statistics to determine the degree of connectivity between populations and species, and determine the most likely demographic scenarios which generally reject for recent hybridization. We find that the combination of WGA and ddRAD allowed us to obtain genomic-level data from microscopic eukaryotes (∼1 millimetre) opening up opportunities for those working with population genomics and phylogenomics in such taxa. The three species share genetic variance, likely from incomplete lineage sorting and ancient admixture. We speculate that the degree of shared variation might underlie morphological similarity in the Atlantic species complex.

Ecological specialisation is hypothesised to play a major role in the evolution of phenotypic diversity, especially following the colonisation of novel habitats. For example, cichlid fishes provide some of the most remarkable evidence for rapid ecological diversification. Here, we capitalised on a recently (≤ 40 years ago) introduced population of red devils (Amphilophus labiatus) in Australia to investigate adaptive phenotypic responses to a novel environment. We used stomach content analyses, morphometrics and laboratory experiments to test for covariation between diet and size of an important trophic trait, lip size. We found that, while maximum lip size in the study population was smaller than in the species’ natural range, the proportions of algae, insects and fish remains in the diet covaried with lip size. However, contrary to predictions, we found no evidence for lip development to be plastic under laboratory conditions in relation to substrate complexity or food manipulation, nor did we find any relationship between lip morphology and feeding performance in adults. Single nucleotide polymorphism data, in turn, suggested that the introduced population has reduced standing genetic variation, which potentially influences both phenotypic plasticity and diversity, in comparison to native populations. Together, the results suggest that morphological variation in a key trophic trait can respond rapidly to diet in a novel environment, despite reduced genetic diversity in the population., This study was funded by a Holsworth Wildlife Endowment, and a Linnean Society of New South Wales Small Research Grant, both awarded to WS. The research alsoreceived support from the SYNTHESYS Project (https://www.synthesys.info/), which is financed by European Community Research Infrastructure Action under the FP7 ‘‘Capacities’’Program (to TKL and MB).

The most successful study systems are built on a foundation of decades of research on the basic biology, ecology and life history of the organisms in question. Combined with new technologies, this can provide a formidable means to address important issues in evolutionary biology and molecular ecology. Littorinid marine snails are a good example of this, with a rich literature on their taxonomy, speciation, thermal tolerance and behavioural adaptations. In August 2017, an international meeting on Littorinid evolution was held at the Tjärnö Marine Research Laboratory in Western Sweden. In this meeting review, I provide a summary of some of the exciting work on parallel evolution, sexual selection and adaptation to environmental stress presented there. I argue that newly available genomic resources present an opportunity for integrating the traditionally divergent fields of speciation and environmental adaptation in Littorinid research.

Differential gene expression can play an important role in phenotypic evolution and divergent adaptation. Although differential gene expression can be caused by both local- and distant-regulatory changes, we know little about their relative contribution to transcriptome evolution in natural populations. Here, we conducted expression quantitative trait loci (eQTL) analysis to investigate the genetic architecture underlying transcriptome divergence between marine and stream ecotypes of threespine sticklebacks (Gasterosteus aculeatus). We identified both local and distant eQTLs, some of which constitute hotspots, regions with a disproportionate number of significant eQTLs relative to the genomic background. The majority of local eQTLs including those in the hotspots caused expression changes consistent with the direction of transcriptomic divergence between ecotypes. Genome scan analysis showed that many local eQTLs overlapped with genomic regions of high differentiation. In contrast, nearly half of the distant eQTLs including those in the hotspots caused opposite expression changes, and few overlapped with regions of high differentiation, indicating that distant eQTLs may act as a constraint of transcriptome evolution. Finally, a comparison between two salinity conditions revealed that nearly half of eQTL hotspots were environment specific, suggesting that analysis of genetic architecture in multiple conditions is essential for predicting response to selection.

Hybridization increases genetic variation, hence hybrid species may have a strong evolutionary potential once their admixed genomes have stabilized and incompatibilities have been purged. Yet, little is known about how such hybrid lineages evolve at the genomic level following their formation, in particular the characteristics of their adaptive potential, i.e. constraints and facilitations of diversification. Here we investigate how the Italian sparrow (Passer italiae), a homoploid hybrid species, has evolved and locally adapted to its variable environment. Using restriction site-associated DNA sequencing (RAD-seq) on several populations across the Italian peninsula, we evaluate how genomic constraints and novel genetic variation have influenced population divergence and adaptation. We show that population divergence within this hybrid species has evolved in response to climatic variation. As in non-hybrid species, climatic differences may even reduce gene flow between populations, suggesting ongoing local adaptation. We report outlier genes associated with adaptation to climatic variation, known to be involved in beak morphology in other species. Most of the strongly divergent loci among Italian sparrow populations seem not to be differentiated between its parent species, the house and Spanish sparrow. Within the parental species, population divergence has occurred mostly in loci where different alleles segregate in the parent species, unlike in the hybrid, suggesting that novel combinations of parental alleles in the hybrid have not necessarily enhanced its evolutionary potential. Rather, our study suggests that constraints linked to incompatibilities may have restricted the evolution of this admixed genome, both during and after hybrid species formation.

The diversity of life on Earth is something that has long fascinated biologists. When we inspect all this variation, two striking patterns emerge. First, organisms appear as if they have almost been “designed” to live the way they do. However, as explained in chapters 4 and 5, the theory of natural selection accounts for this apparent design. The second striking pattern is that variation appears to be non-randomly distributed. That is, it is clustered into groups of individuals that resemble each other and that are recognizably different from other such clusters; species, in other words. To what extent are species biologically meaningful entities in evolution? How do new species originate? What genetic changes occur when one species diverges into two? How is genomic data changing our understanding of speciation? These are among the many questions this chapter addresses. The chapter starts by discussing what constitutes a species.

Science is defined by continual progress and new technologies. This final chapter starts with introducing what it means to sequence and assemble a reference genome. It is easy to forget that the true genome is not linear but has structure and function. In this chapter the genome is explored as a 3D entity—from how it is transcribed, to how proteins interact with it, and finally to how it is actually structured. This also gives an opportunity to focus on epigenetics and how to interpret processes such as DNA methylation in an evolutionary context. The second part of the chapter focuses on ways we can interact with the genome—exploring how we might test the function and role that candidate genes play. The chapter introduces transgenics, in particular the transformative technology of CRISPR/CAS9, and explores how this might change the face of evolutionary biology in the near future.

Evolutionary genetics is the study of how genetic variation leads to evolutionary change. With the recent explosion in the availability of whole genome sequence data, vast quantities of genetic data are being generated at an ever-increasing pace with the result that programming has become an essential tool for researchers. Most importantly, a thorough understanding of evolutionary principles is essential for making sense of this genetic data. This up-to-date textbook covers all the major components of modern evolutionary genetics, carefully explaining fundamental processes such as mutation, natural selection, genetic drift, and speciation, together with their consequences. In addition to the text, study questions are provided to motivate the reader to think and reflect on the concepts in each chapter. Practical experience is essential when it comes to developing an understanding of how to use genetic data to analyze and address interesting questions in the life sciences and how to interpret results in meaningful ways. Throughout the book, a series of online, computer-based tutorials serves as an introduction to programming and analysis of evolutionary genetic data centered on the R programming language, which stands out as an ideal all-purpose platform to handle and analyze such data. The book and its online materials take full advantage of the authors’ own experience in working in a post-genomic revolution world, and introduce readers to the plethora of molecular and analytical methods that have only recently become available.

The fields of evolutionary biology and genetics were founded as separate disciplines in the mid-1800s, largely due to the works of Charles Darwin and Gregor Mendel respectively. It would, however, take decades before biologists finally understood the deep connection between the principles of heredity and the processes of evolution and that neither could be fully understood without the other. This chapter takes a brief look at the history of these disciplines, including how the key concepts, ideas, and technologies, fundamental to all of biology, were discovered and how these have affected our ways of thinking. Many important concepts are foreshadowed here that will be handled at greater depth in later chapters. The chapter ends with a brief review of important methods in contemporary evolutionary genetics and a hint towards future developments in the field.

Error and chance events, random mutations, are necessary prerequisites for evolution to happen. In a perfect world with no mutations there would be no evolution because no genetic variation would be generated that natural selection or genetic drift could work upon. This chapter first reviews how DNA is organized into genomes and genes in bacteria, archaea, and, in greater detail, eukaryotes. A surprising finding is that only a small fraction of the eukaryote genome consists of coding sequence. Evolutionary processes that can explain the presence of large amounts of noncoding DNA and the repetitive structure of the genome are reviewed, with emphasis on the roles that selfish genetic elements and unequal crossing over play. The chapter further explores the mechanisms that cause mutation and how new genes and protein functions originate.

The allelic evolutionary genetic models explored so far are applicable to genetic markers. However, DNA sequences harbor a lot of information about the evolutionary past that would be missed if different sequences were simply treated as different alleles. This chapter introduces some important methods and concepts applicable to the analysis of DNA-sequence data. The null models for analyzing sequence data are derived from the neutral theory of molecular evolution. Historically, however, the neutral theory has made a large impact on evolutionary genetics. Therefore, this chapter starts by reviewing its important contribution. Then, important parameters and statistics for analyzing sequence variation are introduced, including a plethora of neutrality tests. The chapter ends with a cautious focus on the powerful tool of genome scan analysis and its utility for identifying regions of the genomes potentially under selection. This includes a section on more recently derived statistics which incorporate information on haplotype structure.

Adaptations are the products of natural selection—traits that evolved because they proved useful at some level. Often adaptations evolved because they enhanced the survival or reproductive output of individuals, but selection can also operate at other levels—genes, individuals, populations, and species. Sometimes a genetic change has positive effects on all levels. A mutation that increases the survival of its carrier would increase in frequency; populations that become fixed for that allele may be less prone to extinction, which in turn may increase the longevity of that species. Other times there can be conflicting fitness effects at the different levels. This chapter explores the power of natural selection in shaping the living world by investigating the complexities of multilevel selection, biological solutions to heterogeneity and unpredictability in the environment, and how interactions between species can shape evolution. However, the chapter starts by investigating factors that may constrain adaptive evolution.

How can genetics and genomics be used to understand the evolutionary history of organisms? This chapter focuses on such methods. First, the field of phylogenetics is introduced, as a way to visualize and quantify the evolutionary relationships among species. The chapter outlines how we go from aligning DNA sequence data to building gene trees and we argue that “tree-thinking” is fundamentally important for understanding evolution. The chapter also goes beyond phylogenetic trees to focus on phylogeography, i.e. the understanding of evolutionary relationships in a spatial context. More recently, the explosion of genomic data from ancient and modern human populations has made this an extremely exciting field which is transforming our understanding of our own evolutionary history. Before that, though, the chapter reviews how modern phylogenetics has arisen from historical efforts to classify life on Earth.

Evolution is the change in heritable traits of populations over successive generations. At the molecular level this translates into changes in their genetic composition. A general theoretical investigation of how different demographic and evolutionary processes affect genetic variation within and between populations provides us with tools to reconstruct evolutionary history. This is the fundamental purpose of population genetics. This chapter investigates the relationship between allele and genotype frequencies in a hypothetical population that is not subjected to any evolutionary forces—i.e. the Hardy–Weinberg model. Then, one by one, demographic and evolutionary factors such as non-random mating, genetic drift, selection, mutation, and gene flow are introduced to investigate in what ways they affect allele and/or genotype frequencies. The chapter further introduces F-statistics and goodness of fit tests to investigate statistical deviations from expectations.

Natural selection is the scientific explanation for the evolution of adaptations. Wonders of the living world, such as the anatomy and physiology that grants the cheetah its unchallenged running speed; the seductive colors and scents of a flower that are irresistible to its pollinators; and the accuracy and sophistication of sense organs such as the human eye are the ultimate results of this one creative force in evolution. This chapter investigates simple models of natural selection to explore its power in causing evolutionary change. Mathematical techniques including invasion fitness analysis and adaptive landscapes are powerful tools for analyzing such models and for identifying evolutionarily stable and unstable equilibria. The chapter further investigates frequency-dependent selection and evolutionary game theory. An important goal here is to show that selection can take many different forms and yield very different evolutionary outcomes.

Most phenotypic traits are affected by a multitude of genes, which may interact in complex ways. This means that the single locus model explored in chapters 3 and 4 is not always able to capture the full complexity of genetic evolution. In many cases, multiple genes are involved and so this chapter formalizes the analysis of multilocus evolution. Concepts such as linkage disequilibrium and epistasis are introduced, both of which are necessary to properly understand multilocus evolution. The currently highly active field emerging as a result of a crossover between quantitative genetics and genomics is further explored, including methods such as quantitative trait locus (QTL) analysis and genome wide association study (GWAS) that allow phenotypic variation to be associated with likely causative genes and that have made important advances in our understanding of the genetic underpinnings of disease.

Seminal fluid proteins (SFPs) mediate an array of postmating reproductive processes that influence fertilization and fertility. As such, it is widely held that SFPs may contribute to postmating, prezygotic reproductive barriers between closely related taxa. We investigated seminal fluid (SF) diversification in a recently diverged passerine species pair (Passer domesticus and Passer hispaniolensis) using a combination of proteomic and comparative evolutionary genomic approaches. First, we characterized and compared the SF proteome of the two species, revealing consistencies with known aspects of SFP biology and function in other taxa, including the presence and diversification of proteins involved in immunity and sperm maturation. Second, using whole-genome resequencing data, we assessed patterns of genomic differentiation between house and Spanish sparrows. These analyses detected divergent selection on immunity-related SF genes and positive selective sweeps in regions containing a number of SF genes that also exhibited protein abundance diversification between species. Finally, we analyzed the molecular evolution of SFPs across 11 passerine species and found a significantly higher rate of positive selection in SFPs compared with the rest of the genome, as well as significant enrichments for functional pathways related to immunity in the set of positively selected SF genes. Our results suggest that selection on immunity pathways is an important determinant of passerine SF composition and evolution. Assessing the role of immunity genes in speciation in other recently diverged taxa should be prioritized given the potential role for immunity-related proteins in reproductive incompatibilities in Passer sparrows.

Smallpox, caused by the variola virus (VARV), was a highly virulent disease with high mortality rates causing a major threat for global human health until its successful eradication in 1980. Despite previously published historic and modern VARV genomes, its past dissemination and diversity remain debated. To understand the evolutionary history of VARV with respect to historic and modern VARV genetic variation in Europe, we sequenced a VARV genome from a well-described eighteenth-century case from England (specimen P328). In our phylogenetic analysis, the new genome falls between the modern strains and another historic strain from Lithuania, supporting previous claims of larger diversity in early modern Europe compared to the twentieth century. Our analyses also resolve a previous controversy regarding the common ancestor between modern and historic strains by confirming a later date around the seventeenth century. Overall, our results point to the benefit of historic genomes for better resolution of past VARV diversity and highlight the value of such historic genomes from around the world to further understand the evolutionary history of smallpox as well as related diseases.This article is part of the theme issue ‘Insights into health and disease from ancient biomolecules’.

Speciation is a continuous process and analysis of species pairs at different stages of divergence provides insight into how it unfolds. Previous genomic studies on young species pairs have revealed peaks of divergence and heterogeneous genomic differentiation. Yet less known is how localised peaks of differentiation progress to genome-wide divergence during the later stages of speciation in the presence of persistent gene flow. Spanning the speciation continuum, stickleback species pairs are ideal for investigating how genomic divergence builds up during speciation. However, attention has largely focused on young postglacial species pairs, with little knowledge of the genomic signatures of divergence and introgression in older stickleback systems. The Japanese stickleback species pair, composed of the Pacific Ocean three-spined stickleback (Gasterosteus aculeatus) and the Japan Sea stickleback (G. nipponicus), which co-occur in the Japanese islands, is at a late stage of speciation. Divergence likely started well before the end of the last glacial period and crosses between Japan Sea females and Pacific Ocean males result in hybrid male sterility. Here we use coalescent analyses and Approximate Bayesian Computation to show that the two species split approximately 0.68–1 million years ago but that they have continued to exchange genes at a low rate throughout divergence. Population genomic data revealed that, despite gene flow, a high level of genomic differentiation is maintained across the majority of the genome. However, we identified multiple, small regions of introgression, occurring mainly in areas of low recombination rate. Our results demonstrate that a high level of genome-wide divergence can establish in the face of persistent introgression and that gene flow can be localized to small genomic regions at the later stages of speciation with gene flow., Author summary When species evolve, reproductive isolation leads to a build-up of differentiation in the genome where genes involved in the process occur. Spanning the speciation continuum, stickleback species pairs are ideal for investigating how genomic divergence accumulates during speciation. However, much of our understanding of stickleback speciation comes from early stage divergence, with relatively few examples from more divergent species pairs that still exchange genes. To address this, we focused on Pacific Ocean and Japan Sea sticklebacks, which co-occur in the Japanese islands. We established that they are the oldest and most divergent known stickleback species pair, that they evolved in the face of gene flow and that this gene flow is still on going. We found introgression is confined to small, localised genomic regions where recombination rate is high. Our results show high divergence can be maintained between species, despite extensive gene flow.

Background Marine threespine sticklebacks colonized and adapted to brackish and freshwater environments since the last Pleistocene glacial. Throughout the Holarctic, three lateral plate morphs are observed; the low, partial and completely plated morph. We test if the three plate morphs in the brackish water Lake Engervann, Norway, differ in body size, trophic morphology (gill raker number and length), niche (stable isotopes; δ15N, δ13C, and parasites (Theristina gasterostei, Trematoda spp.)), genetic structure (microsatellites) and the lateral-plate encoding Stn382 (Ectodysplasin) gene. We examine differences temporally (autumn 2006/spring 2007) and spatially (upper/lower sections of the lake – reflecting low versus high salinity). Results All morphs belonged to one gene pool. The complete morph was larger than the low plated, with the partial morph intermediate. The number of lateral plates ranged 8–71, with means of 64.2 for complete, 40.3 for partial, and 14.9 for low plated morph. Stickleback δ15N was higher in the lower lake section, while δ13C was higher in the upper section. Stickleback isotopic values were greater in autumn. The low plated morph had larger variances in δ15N and δ13C than the other morphs. Sticklebacks in the upper section had more T. gasterostei than in the lower section which had more Trematoda spp. Sticklebacks had less T. gasterostei, but more Trematoda spp. in autumn than spring. Sticklebacks with few and short rakers had more T. gasterostei, while sticklebacks with longer rakers had more Trematoda. spp. Stickleback with higher δ15N values had more T. gasterostei, while sticklebacks with higher δ15N and δ13C values had more Trematoda spp. The low plated morph had fewer Trematoda spp. than other morphs. Conclusions Trait-ecology associations may imply that the three lateral plate morphs in the brackish water lagoon of Lake Engervann are experiencing ongoing divergent selection for niche and migratory life history strategies under high gene flow. As such, the brackish water zone may generally act as a generator of genomic diversity to be selected upon in the different environments where threespine sticklebacks can live. Electronic supplementary material The online version of this article (10.1186/s12862-018-1128-y) contains supplementary material, which is available to authorized users.

House sparrows (Passer domesticus) are a hugely successful anthrodependent species; occurring on nearly every continent. Yet, despite their ubiquity and familiarity to humans, surprisingly little is known about their origins. We sought to investigate the evolutionary history of the house sparrow and identify the processes involved in its transition to a human-commensal niche. We used a whole genome resequencing dataset of 120 individuals from three Eurasian species, including three populations of Bactrianus sparrows, a non-commensal, divergent house sparrow lineage occurring in the Near East. Coalescent modelling supports a split between house and Bactrianus sparrow 11 Kya and an expansion in the house sparrow at 6 Kya, consistent with the spread of agriculture following the Neolithic revolution. Commensal house sparrows therefore likely moved into Europe with the spread of agriculture following this period. Using the Bactrianus sparrow as a proxy for a pre-commensal, ancestral house population, we performed a comparative genome scan to identify genes potentially involved with adaptation to an anthropogenic niche. We identified potential signatures of recent, positive selection in the genome of the commensal house sparrow that are absent in Bactrianus populations. The strongest selected region encompasses two major candidate genes;COL11A—which regulates craniofacial and skull development andAMY2A, part of the amylase gene family which has previously been linked to adaptation to high-starch diets in humans and dogs. Our work examines human-commensalism in an evolutionary framework, identifies genomic regions likely involved in rapid adaptation to this new niche and ties the evolution of this species to the development of modern human civilization.

International audience; Speciation, the evolution of reproductive isolation among populations, is continuous, complex, and involves multiple, interacting barriers. Until it is complete, the effects of this process vary along the genome and can lead to a heterogeneous genomic landscape with peaks and troughs of differentiation and divergence. When gene flow occurs during speciation, barriers restricting gene flow locally in the genome lead to patterns of heterogeneity. However, genomic heterogeneity can also be produced or modified by variation in factors such as background selection and selective sweeps, recombination and mutation rate variation, and heterogeneous gene density. Extracting the effects of gene flow, divergent selection and reproductive isolation from such modifying factors presents a major challenge to speciation genomics. We argue one of the principal aims of the field is to identify the barrier loci involved in limiting gene flow. We first summarize the expected signatures of selection at barrier loci, at the genomic regions linked to them and across the entire genome. We then discuss the modifying factors that complicate the interpretation of the observed genomic landscape. Finally, we end with a road map for future speciation research: a proposal for how to account for these modifying factors and to progress towards understanding the nature of barrier loci. Despite the difficulties of interpreting empirical data, we argue that the availability of promising technical and analytical methods will shed further light on the important roles that gene flow and divergent selection have in shaping the genomic landscape of speciation.

SummaryRecent genomic investigations have revealed hybridization to be an important source of variation, the working material of natural selection1,2. Hybridization can spur adaptive radiations3, transfer adaptive variation across species boundaries4, and generate species with novel niches5. Yet, the limits to viable hybrid genome formation are poorly understood. Here we investigated to what extent hybrid genomes are free to evolve or whether they are restricted to a specific combination of parental alleles by sequencing the genomes of four isolated island populations of the homoploid hybrid Italian sparrowPasser italiae6,7. Based on 61 Italian sparrow genomes from Crete, Corsica, Sicily and Malta, and 10 genomes of each of the parent speciesP. domesticusandP. hispaniolensis,we report that a variety of novel and fully functional hybrid genomic combinations have arisen on the different islands, with differentiation in candidate genes for beak shape and plumage colour. There are limits to successful genome fusion, however, as certain genomic regions are invariably inherited from the same parent species. These regions are overrepresented on the Z-chromosome and harbour candidate incompatibility loci, including DNA-repair and mito-nuclear genes; loci that may drive the general reduction of introgression on sex chromosomes8. Our findings demonstrate that hybridization is a potent process for generating novel variation, but variation is limited by DNA-repair and mito-nuclear genes, which play an important role in reproductive isolation and thus contribute to speciation.

Parallel evolution of similar traits by independent populations in similar environments is considered strong evidence for adaptation by natural selection. Often, however, replicate populations in similar environments do not all evolve in the same way, thus deviating from any single, predominant outcome of evolution. This variation might arise from non-adaptive, population-specific effects of genetic drift, gene flow or limited genetic variation. Alternatively, these deviations from parallel evolution might also reflect predictable adaptation to cryptic environmental heterogeneity within discrete habitat categories. Here, we show that deviations from parallel evolution are the consequence of environmental variation within habitats combined with variation in gene flow. Threespine stickleback (Gasterosteus aculeatus) in adjoining lake and stream habitats (a lake-stream 'pair') diverge phenotypically, yet the direction and magnitude of this divergence is not always fully parallel among 16 replicate pairs. We found that the multivariate direction of lake-stream morphological divergence was less parallel between pairs whose environmental differences were less parallel. Thus, environmental heterogeneity among lake-stream pairs contributes to deviations from parallel evolution. Additionally, likely genomic targets of selection were more parallel between environmentally more similar pairs. In contrast, variation in the magnitude of lake-stream divergence (independent of direction) was better explained by differences in lake-stream gene flow; pairs with greater lake-stream gene flow were less morphologically diverged. Thus, both adaptive and non-adaptive processes work concurrently to generate a continuum of parallel evolution across lake-stream stickleback population pairs.

Genomic mosaicism and novel divergence have facilitated the creation and maintenance of a hybrid species, the Italian sparrow., Hybridization is widespread in nature and, in some instances, can result in the formation of a new hybrid species. We investigate the genetic foundation of this poorly understood process through whole-genome analysis of the hybrid Italian sparrow and its progenitors. We find overall balanced yet heterogeneous levels of contribution from each parent species throughout the hybrid genome and identify areas of novel divergence in the hybrid species exhibiting signals consistent with balancing selection. High-divergence areas are disproportionately located on the Z chromosome and overrepresented in gene networks relating to key traits separating the focal species, which are likely involved in reproductive barriers and/or species-specific adaptations. Of special interest are genes and functional groups known to affect body patterning, beak morphology, and the immune system, which are important features of diversification and fitness. We show that a combination of mosaic parental inheritance and novel divergence within the hybrid lineage has facilitated the origin and maintenance of an avian hybrid species.