Carole M. Smadja

Hybridization and speciation

Hybridization has many and varied impacts on the process of speciation. Hybridization may slow or reverse differentiation by allowing gene flow and recombination. It may accelerate speciation via adaptive introgression or cause near‐instantaneous speciation by allopolyploidization. It may have multiple effects at different stages and in different spatial contexts within a single speciation event. We offer a perspective on the context and evolutionary significance of hybridization during speciation, highlighting issues of current interest and debate. In secondary contact zones, it is uncertain if barriers to gene flow will be strengthened or broken down due to recombination and gene flow. Theory and empirical evidence suggest the latter is more likely, except within and around strongly selected genomic regions. Hybridization may contribute to speciation through the formation of new hybrid taxa, whereas introgression of a few loci may promote adaptive divergence and so facilitate speciation. Gene regulatory networks, epigenetic effects and the evolution of selfish genetic material in the genome suggest that the Dobzhansky–Muller model of hybrid incompatibilities requires a broader interpretation. Finally, although the incidence of reinforcement remains uncertain, this and other interactions in areas of sympatry may have knock‐on effects on speciation both within and outside regions of hybridization.

Adaptation genomics: the next generation

Understanding the genetics of how organisms adapt to changing environments is a fundamental topic in modern evolutionary ecology. The field is currently progressing rapidly because of advances in genomics technologies, especially DNA sequencing. The aim of this review is to first briefly summarise how next generation sequencing (NGS) has transformed our ability to identify the genes underpinning adaptation. We then demonstrate how the application of these genomic tools to ecological model species means that we can start addressing some of the questions that have puzzled ecological geneticists for decades such as: How many genes are involved in adaptation? What types of genetic variation are responsible for adaptation? Does adaptation utilise pre-existing genetic variation or does it require new mutations to arise following an environmental change?

On the scent of speciation: the chemosensory system and its role in premating isolation.

Chemosensory speciation is characterized by the evolution of barriers to genetic exchange that involve chemosensory systems and chemical signals. Here, we review some representative studies documenting chemosensory speciation in an attempt to evaluate the importance and the different aspects of the process in nature and to gain insights into the genetic basis and the evolutionary mechanisms of chemosensory trait divergence. Although most studies of chemosensory speciation concern sexual isolation mediated by pheromone divergence, especially in Drosophila and moth species, other chemically based behaviours (habitat choice, pollinator attraction) can also play an important role in speciation and are likely to do so in a wide range of invertebrate and vertebrate species. Adaptive divergence of chemosensory traits in response to factors such as pollinators, hosts and conspecifics commonly drives the evolution of chemical prezygotic barriers. Although the genetic basis of chemosensory speciation remains largely unknown, genomic approaches to chemosensory gene families and to enzymes involved in biosynthetic pathways of signal compounds now provide new opportunities to dissect the genetic basis of these complex traits and of their divergence among taxa.

A framework for comparing processes of speciation in the presence of gene flow

How common is speciation‐with‐gene‐flow? How much does gene flow impact on speciation? To answer questions like these requires understanding of the common obstacles to evolving reproductive isolation in the face of gene flow and the factors that favour this crucial step. We provide a common framework for the ways in which gene flow opposes speciation and the potential conditions that may ease divergence. This framework is centred on the challenge shared by most scenarios of speciation‐with‐gene‐flow, i.e. the need for coupling among different components of reproductive isolation. Using this structure, we review and compare the factors favouring speciation with the intention of providing a more integrated picture of speciation‐with‐gene‐flow.

LARGE-SCALE CANDIDATE GENE SCAN REVEALS THE ROLE OF CHEMORECEPTOR GENES IN HOST PLANT SPECIALIZATION AND SPECIATION IN THE PEA APHID

Understanding the drivers of speciation is critical to interpreting patterns of biodiversity. The identification of the genetic changes underlying adaptation and reproductive isolation is necessary to link barriers to gene flow to the causal origins of divergence. Here, we present a novel approach to the genetics of speciation, which should complement the commonly used approaches of quantitative trait locus mapping and genome‐wide scans for selection. We present a large‐scale candidate gene approach by means of sequence capture, applied to identifying the genetic changes underlying reproductive isolation in the pea aphid, a model system for the study of ecological speciation. Targeted resequencing enabled us to scale up the candidate gene approach, specifically testing for the role of chemosensory gene families in host plant specialization. Screening for the signature of divergence under selection at 172 candidate and noncandidate loci, we revealed a handful of loci that show high levels of differentiation among host races, which almost all correspond to odorant and gustatory receptor genes. This study offers the first indication that some chemoreceptor genes, often tightly linked together in the genome, could play a key role in local adaptation and reproductive isolation in the pea aphid and potentially other phytophagous insects. Our approach opens a new route toward the functional genomics of ecological speciation.

Asymmetrical reproductive character displacement in the house mouse.

Our study addressed reproductive character displacement between two subspecies of the house mouse, Mus musculus musculus and Mus musculus domesticus that hybridize in Europe along a zone where selection against hybridization is known to occur. Based on a multi‐population approach, we investigated spatial patterns of divergence of mate preference in the two taxa. Mate preference was significantly higher in the contact zone than in allopatry in both subspecies, suggesting that reproductive character displacement occurs. Moreover, patterns of preference were stronger in M. m. musculus than in M. m. domesticus, indicating an asymmetrical divergence between the two. In the context of selection against hybridization, our results may provide empirical support for the hypothesis of reinforcement in a parapatric hybrid zone. We discuss factors that could explain the asymmetrical pattern of divergence and the possible impact of a unimodal structure on the maintenance of premating divergence between the two subspecies.

Strong premating divergence in a unimodal hybrid zone between two subspecies of the house mouse

Although selection against hybridization is expected to generate prezygotic divergence in unimodal hybrid zones, such a pattern has been seldom described. This study aims to better understand how prezygotic mechanisms may evolve in such zones. We investigated prezygotic divergence between populations of two subspecies of mice (Mus musculus musculus and M. m. domesticus) located at the edges of their unimodal hybrid zone in Denmark, and we developed an original multiple‐population choice‐test design, which allows assessment of within and between subspecies variation. Our study demonstrates that a strong assortative preference characterises one of the two subspecies (musculus) and that urinary signals are involved in this subspecies recognition. Taking into account the specific genetic and geographical characteristics of the Danish hybrid zone, we discuss the influence of the above pattern on its fate and the mechanisms that could have favoured this prezygotic divergence, among which the role of recombined populations constituting the core of the zone.

Reproductive character displacement is not the only possible outcome of reinforcement

We study the form of the clines in a female mating preference and male display trait using simulations of a hybrid zone. Allopatric populations of two species are connected by demes in a stepping stone arrangement. Results show that reproductive character displacement (a pattern of increased prezygotic isolation in sympatry compared with allopatry) may or may not result when there is reinforcement (defined here as the strengthening of prezygotic isolation as a result of selection against hybrids, relative to the amount of prezygotic isolation present when hybrids are not selected against). Further, reproductive character displacement of the preference may or may not occur when it occurs in the male display. We conclude that the absence of reproductive character displacement is not evidence against the operation of reinforcement.

Dynamics of copy number variation in host races of the pea aphid

Copy number variation (CNV) makes a major contribution to overall genetic variation and is suspected to play an important role in adaptation. However, aside from a few model species, the extent of CNV in natural populations has seldom been investigated. Here, we report on CNV in the pea aphid Acyrthosiphon pisum, a powerful system for studying the genetic architecture of host-plant adaptation and speciation thanks to multiple host races forming a continuum of genetic divergence. Recent studies have highlighted the potential importance of chemosensory genes, including the gustatory and olfactory receptor gene families (Gr and Or, respectively), in the process of host race formation. We used targeted resequencing to achieve a very high depth of coverage, and thereby revealed the extent of CNV of 434 genes, including 150 chemosensory genes, in 104 individuals distributed across eight host races of the pea aphid. We found that CNV was widespread in our global sample, with a significantly higher occurrence in multigene families, especially in Ors. We also observed a decrease in the gene probability of being completely duplicated or deleted (CDD) with increase in coding sequence length. Genes with CDD variants were usually more polymorphic for copy number, especially in the P450 gene family where toxin resistance may be related to gene dosage. We found that Gr were overrepresented among genes discriminating host races, as were CDD genes and pseudogenes. Our observations shed new light on CNV dynamics and are consistent with CNV playing a role in both local adaptation and speciation.

A comparative analysis of the mechanisms underlying speciation on Lord Howe Island.

On Lord Howe Island, speciation is thought to have taken place in situ in a diverse array of distantly related plant taxa (Metrosideros, Howea and Coprosma; Proc. Natl Acad. Sci. USA 108, 2011, 13188). We now investigate whether the speciation processes were driven by divergent natural selection in each genus by examining the extent of ecological and genetic divergence. We present new and extensive, ecological and genetic data for all three genera. Consistent with ecologically driven speciation, outlier loci were detected using genome scan methods. This mechanism is supported by individual‐based analyses of genotype–environment correlations within species, demonstrating that local adaptation is currently widespread on the island. Genetic analyses show that prezygotic isolating barriers within species are currently insufficiently strong to allow further population differentiation. Interspecific hybridization was found in both Howea and Coprosma, and species distribution modelling indicates that competitive exclusion may result in selection against admixed individuals. Colonization of new niches, partly fuelled by the rapid generation of new adaptive genotypes via hybridization, appears to have resulted in the adaptive radiation in Coprosma – supporting the ‘Syngameon hypothesis’.