Revisiting the particular role of host shifts in initiating insect speciation

The notion that shifts to new hosts can initiate insect speciation is more than 150 years old, yet widespread conflation with paradigms of sympatric speciation has led to confusion about how much support exists for this hypothesis. Here, we review 85 insect systems and evaluate the relationship between host shifting, reproductive isolation, and speciation. We sort insects into five categories: (1) systems in which a host shift has initiated speciation; (2) systems in which a host shift has made a contribution to speciation; (3) systems in which a host shift has caused the evolution of new reproductive isolating barriers; (4) systems with host‐associated genetic differences; and (5) systems with no evidence of host‐associated genetic differences. We find host‐associated genetic structure in 65 systems, 43 of which show that host shifts have resulted in the evolution of new reproductive barriers. Twenty‐six of the latter also support a role for host shifts in speciation, including eight studies that definitively support the hypothesis that a host shift has initiated speciation. While this review is agnostic as to the fraction of all insect speciation events to which host shifts have contributed, it clarifies that host shifts absolutely can and do initiate speciation.     

Does a predatory insect contribute to the divergence between cave- and surface-adapted fish populations?

Immigrant inviability, where individuals from foreign, ecologically divergent habitats are less likely to survive, can restrict gene flow among diverging populations and result in speciation. I investigated whether a predatory aquatic insect (Belostoma sp.) selects against migrants between cave and surface populations of a fish (Poecilia mexicana). Cavefish were more susceptible to attacks in the light, whereas surface fish were more susceptible in darkness. Environmentally dependent susceptibility to attacks may thus contribute to genetic and phenotypic differentiation between the populations. This study highlights how predation—in this case in conjunction with differences in other environmental factors—can be an important driver in speciation.     

A field reciprocal transplant experiment reveals asymmetric costs of migration between lake and river ecotypes of three‐spined sticklebacks (Gasterosteus aculeatus)

Theory of local adaptation predicts that nonadapted migrants will suffer increased costs compared to local residents. Ultimately this process can result in the reduction of gene flow and culminate in speciation. Here, we experimentally investigated the relative fitness of migrants in foreign habitats, focusing on diverging lake and river ecotypes of three‐spined sticklebacks. A reciprocal transplant experiment performed in the field revealed asymmetric costs of migration: whereas mortality of river fish was increased under lake conditions, lake migrants suffered from reduced growth relative to river residents. Selection against migrants thus involved different traits in each habitat but generally contributed to bidirectional reduction in gene flow. Focusing particularly on the parasitic environments, migrant fish differed from resident fish in the parasite community they harboured. This pattern correlated with both cellular phenotypes of innate immunity as well as with allelic variation at the genes of the major histocompatibility complex. In addition to showing the costs of migration in three‐spined sticklebacks, this study highlights the role of asymmetric selection particularly from parasitism in genotype sorting and in the emergence of local adaptation.     

Immigrant inviability produces a strong barrier to gene flow between parapatric ecotypes of Senecio lautus

Speciation proceeds when gene exchange is prevented between populations. Determining the different barriers preventing gene flow can therefore give insights into the factors driving and maintaining species boundaries. These reproductive barriers may result from intrinsic genetic incompatibilities between populations, from extrinsic environmental differences between populations, or a combination of both mechanisms. We investigated the potential barriers to gene exchange between three adjacent ecotypes of an Australian wildflower to determine the strength of individual barriers and the degree of overall isolation between populations. We found almost complete isolation between the three populations mainly due to premating extrinsic barriers. Intrinsic genetic barriers were weak and variable among populations. There were asymmetries in some intrinsic barriers due to the origin of cytoplasm in hybrids. Overall, these results suggest that reproductive isolation between these three populations is almost complete despite the absence of geographic barriers, and that the main drivers of this isolation are ecologically based, consistent with the mechanisms underlying ecological speciation.     

Thermal adaptation and ecological speciation

Ecological speciation is defined as the emergence of reproductive isolation as a direct or indirect consequence of divergent ecological adaptation. Several empirical examples of ecological speciation have been reported in the literature which very often involve adaptation to biotic resources. In this review, we investigate whether adaptation to different thermal habitats could also promote speciation and try to assess the importance of such processes in nature. Our survey of the literature identified 16 animal and plant systems where divergent thermal adaptation may underlie (partial) reproductive isolation between populations or may allow the stable coexistence of sibling taxa. In many of the systems, the differentially adapted populations have a parapatric distribution along an environmental gradient. Isolation often involves extrinsic selection against locally maladapted parental or hybrid genotypes, and additional pre- or postzygotic barriers may be important. Together, the identified examples strongly suggest that divergent selection between thermal environments is often strong enough to maintain a bimodal genotype distribution upon secondary contact. What is less clear from the available data is whether it can also be strong enough to allow ecological speciation in the face of gene flow through reinforcement-like processes. It is possible that intrinsic features of thermal gradients or the genetic basis of thermal adaptation make such reinforcement-like processes unlikely but it is equally possible that pertinent systems are understudied. Overall, our literature survey highlights (once again) the dearth of studies that investigate similar incipient species along the continuum from initial divergence to full reproductive isolation and studies that investigate all possible reproductive barriers in a given system.     

Ecological speciation in phytophagous insects

Divergent natural selection has been shown to promote speciation in a wide range of taxa. For example, adaptation to different ecological environments, via divergent selection, can result in the evolution of reproductive incompatibility between populations. Phytophagous insects have been at the forefront of these investigations of 'ecological speciation' and it is clear that adaptation to different host plants can promote insect speciation. However, much remains unknown. For example, there is abundant variability in the extent to which divergent selection promotes speciation, the sources of divergent selection, the types of reproductive barriers involved, and the genetic basis of divergent adaptation. We review these factors here. Several findings emerge, including the observation that although numerous different sources of divergent selection and reproductive isolation can be involved in insect speciation, their order of evolution and relative importance are poorly understood. Another finding is that the genetic basis of host preference and performance can involve loci of major effect and opposing dominance, factors which might facilitate speciation in the face of gene flow. In addition, we raise a number of other recent issues relating to phytophagous insect speciation, such as alternatives to ecological speciation, the geography of speciation, and the molecular signatures of speciation. Throughout, we aim to both synthesize what is known, as well as highlight areas where future work is especially needed.     

THE LANGUAGE OF SPECIATION

The literature on speciation has expanded dramatically in recent years, catalyzed by the emergence of new conceptual frameworks, new theoretical approaches, and new methods for characterizing pattern and inferring process. As a consequence, the language used to describe the speciation process has become more complex. Increasing complexity may be an accurate reflection of current thinking with respect to how phenotypic differences limit gene flow, how selection results in the evolution of reproductive isolation, and genetic changes that contribute to speciation. However, increased language complexity has come at a cost; old definitions have been reconfigured and new terms have been introduced. In some instances, the introduction of new terminology has failed to recognize historical usage, leading to unnecessary ambiguity and redundancy. Although the writings of Mayr and Dobzhansky remain a reference point in the language of speciation, the last decades of the 20th century saw substantial changes in our thinking about the speciation process. During that period, the language of speciation remained relatively stable. In contrast, the first decade of the 21st century has witnessed a remarkable expansion of the language of speciation. Here, the origin and evolution of ideas about speciation are viewed through the lens of changing language use.     

Strong postmating reproductive isolation in Mimulus section Eunanus

Postmating reproductive isolation can help maintain species boundaries when premating barriers to reproduction are incomplete. The strength and identity of postmating reproductive barriers are highly variable among diverging species, leading to questions about their genetic basis and evolutionary drivers. These questions have been tackled in model systems but are less often addressed with broader phylogenetic resolution. In this study we analyse patterns of genetic divergence alongside direct measures of postmating reproductive barriers in an overlooked group of sympatric species within the model monkeyflower genus, Mimulus. Within this Mimulus brevipes species group, we find substantial divergence among species, including a cryptic genetic lineage. However, rampant gene discordance and ancient signals of introgression suggest a complex history of divergence. In addition, we find multiple strong postmating barriers, including postmating prezygotic isolation, hybrid seed inviability and hybrid male sterility. M. brevipes and M. fremontii have substantial but incomplete postmating isolation. For all other tested species pairs, we find essentially complete postmating isolation. Hybrid seed inviability appears linked to differences in seed size, providing a window into possible developmental mechanisms underlying this reproductive barrier. While geographic proximity and incomplete mating isolation may have allowed gene flow within this group in the distant past, strong postmating reproductive barriers today have likely played a key role in preventing ongoing introgression. By producing foundational information about reproductive isolation and genomic divergence in this understudied group, we add new diversity and phylogenetic resolution to our understanding of the mechanisms of plant speciation.     

基因流存在条件下的物种形成研究述评:生殖隔离机制进化

物种形成过程是生物多样性形成的基础, 长期以来一直是进化生物学的中心议题之一。传统的异域物种形成理论认为, 地理隔离是物种分化的主要决定因子, 物种形成只有在种群之间存在地理隔离的情况下才能发生。近年来, 随着种群基因组学的发展和溯祖理论分析方法的完善, 种群间存在基因流情况下的物种形成成为进化生物学领域新的研究焦点。物种形成过程中是否有基因流的发生?基因流如何影响物种的形成与分化?基因流存在条件下物种形成的生殖隔离机制是什么?根据已发表的相关文献资料, 作者综述了当前物种形成研究中基因流的时间和空间分布模式、基因流对物种分化的影响以及生殖隔离机制形成等问题, 指出基因流存在条件下的物种形成可能是自然界普遍发生的一种模式。     

Divergent host plant specialization as the critical driving force in speciation between populations of a phytophagous ladybird beetle

Detecting the isolating barrier that arises earliest in speciation is critically important to understanding the mechanism of species formation. We tested isolating barriers between host races of a phytophagous ladybird beetle, Henosepilachna diekei (Coleoptera: Coccinellidae: Epilachnine), that occur sympatrically on distinct host plants. We conducted field surveys for the distribution of the beetles and host plants, rearing experiments to measure six potential isolating factors (adult host preference, adult and larval host performance, sexual isolation, egg hatchability, F(1) hybrid inviability, and sexual selection against F(1) hybrids), and molecular analyses of mitochondrial ND2 and the nuclear ITS2 sequences. We found significant genetic divergence between the host races, and extremely divergent host preference (i.e. habitat isolation) and host performance (i.e. immigrant inviability), but no other isolating barriers. The fidelity to particular host plants arises first and alone can prevent gene flow between differentiating populations of phytophagous specialists.     

生态物种形成及其研究进展

物种形成是基本的进化过程, 也是生物多样性形成的基础。自然选择可以导致新物种的产生。生态物种形成是指以生态为基础的歧化选择使不同群体分化产生生殖隔离的物种形成过程。本文首先回顾了生态物种形成的研究历史, 并详细介绍了生态物种形成的3个要素, 即歧化选择的来源、生殖隔离的形式以及关联歧化选择与生殖隔离的遗传机制。歧化选择的来源主要包括不同的环境或生态位、不同形式的性选择, 以及群体间的相互作用。生殖隔离的形式多种多样, 我们总结了合子前和合子后隔离的遗传学机制以及在生态物种形成中起到的作用。控制适应性性状的基因与导致生殖隔离的基因可以通过基因多效性或连锁不平衡相互关联起来。借助于第二代测序技术, 研究者可以对生态物种形成的遗传学与基因组学基础进行研究。此外, 本文还总结了生态物种形成领域最新的研究进展, 包括平行进化的全基因组基础, 以及基因流影响群体分化的理论基础。通过归纳比较由下至上和由上至下这两种不同的研究思路, 作者认为这两种思路的结合可以为生态物种形成基因的筛选提供更有力也更精确的方法。同时, 作者还提出生态物种形成的研究应该基于更好的表型描述以及更完整的基因组信息, 研究的物种也应该具有更广泛的代表性。     

The accumulation of reproductive barriers during speciation: postmating barriers in two behaviorally isolated species of darters (Percidae: Etheostoma)

Identifying the manner in which reproductive barriers accumulate during lineage divergence is central to establishing general principles of species formation. One outstanding question is which isolating mechanisms form the first complete barrier to gene flow in a given lineage or under a particular set of conditions. To identify these initial reproductive barriers requires examining lineages in very early stages of divergence, before multiple reproductive barriers have evolved to completion. We quantified the strength of three postmating barriers in a pair of darter species and compared these estimates to each other and to the strength of behavioral isolation (BI) reported in a previous study. Results reveal no evidence of gametic incompatibility but intermediate levels of conspecific sperm precedence and hybrid inviability. As BI is nearly complete, our analysis comparing the strength of multiple reproductive barriers implicates the evolution of mate choice as central to both the origin and maintenance of these species. Further examination of ecological isolation and hybrid sterility is necessary to determine the role of these barriers in darter speciation.     

The genic view of the process of speciation

The unit of adaptation is usually thought to be a gene or set of interacting genes, rather than the whole genome, and this may be true of species differentiation. Defining species on the basis of reproductive isolation (RI), on the other hand, is a concept best applied to the entire genome. The biological species concept (BSC; 84 ) stresses the isolation aspect of speciation on the basis of two fundamental genetic assumptions – the number of loci underlying species differentiation is large and the whole genome behaves as a cohesive, or coadapted genetic unit. Under these tenets, the exchange of any part of the genomes between diverging groups is thought to destroy their integrity. Hence, the maintenance of each species’ genome cohesiveness by isolating mechanisms has become the central concept of species. In contrast, the Darwinian view of speciation is about differential adaptation to different natural or sexual environments. RI is viewed as an important by product of differential adaptation and complete RI across the whole genome need not be considered as the most central criterion of speciation. The emphasis on natural and sexual selection thus makes the Darwinian view compatible with the modern genic concept of evolution. Genetic and molecular analyses of speciation in the last decade have yielded surprisingly strong support for the neo‐Darwinian view of extensive genetic differentiation and epistasis during speciation. However, the extent falls short of what BSC requires in order to achieve whole‐genome ‘cohesiveness’. Empirical observations suggest that the gene is the unit of species differentiation. Significantly, the genetic architecture underlying RI, the patterns of species hybridization and the molecular signature of speciation genes all appear to support the view that RI is one of the manifestations of differential adaptation, as 34 , Chap. 8) suggested. The nature of this adaptation may be as much the result of sexual selection as natural selection. In the light of studies since its early days, BSC may now need a major revision by shifting the emphasis from isolation at the level of whole genome to differential adaptation at the genic level. With this revision, BSC would in fact be close to Darwin’s original concept of speciation.     

Quantified reproductive isolation in Heliconius butterflies: Implications for introgression and hybrid speciation

Heliconius butterflies have become a model for the study of speciation with gene flow. For adaptive introgression to take place, there must be incomplete barriers to gene exchange that allow interspecific hybridization and multiple generations of backcrossing. The recent publication of estimates of individual components of reproductive isolation between several species of butterflies in the Heliconius melpomene–H. cydno clade allowed us to calculate total reproductive isolation estimates for these species. According to these estimates, the butterflies are not as promiscuous as has been implied. Differences between species are maintained by intrinsic mechanisms, while reproductive isolation of geographical races within species is mainly due to allopatry. We discuss the implications of this strong isolation for basic aspects of the hybrid speciation with introgression hypothesis.     

被子植物同域物种形成研究进展

同域物种形成是指在缺少地理隔离的情况下分化出新种,相比异域物种形成更为罕见,存在较多的研究空白.该文分析了近十年来与被子植物同域物种形成相关的国内外研究,着重论述同域物种形成的影响因素和种对间的生殖隔离.考虑到历史上的地理隔离难以确定,加之种对间亲缘关系很近,同域物种的判定容易引发争议.其成因可分为生态因素和突变因素:...     

The genomic bases of morphological divergence and reproductive isolation driven by ecological speciation in Senecio (Asteraceae)

Ecological speciation, driven by adaptation to contrasting environments, provides an attractive opportunity to study the formation of distinct species, and the role of selection and genomic divergence in this process. Here, we focus on a particularly clear‐cut case of ecological speciation to reveal the genomic bases of reproductive isolation and morphological differences between closely related Senecio species, whose recent divergence within the last ~200 000 years was likely driven by the uplift of Mt. Etna (Sicily). These species form a hybrid zone, yet remain morphologically and ecologically distinct, despite active gene exchange. Here, we report a high‐density genetic map of the Senecio genome and map hybrid breakdown to one large and several small quantitative trait loci (QTL). Loci under diversifying selection cluster in three 5 cM regions which are characterized by a significant increase in relative (F_ST), but not absolute (d_XY), interspecific differentiation. They also correspond to some of the regions of greatest marker density, possibly corresponding to ‘cold‐spots’ of recombination, such as centromeres or chromosomal inversions. Morphological QTL for leaf and floral traits overlap these clusters. We also detected three genomic regions with significant transmission ratio distortion (TRD), possibly indicating accumulation of intrinsic genetic incompatibilities between these recently diverged species. One of the TRD regions overlapped with a cluster of high species differentiation, and another overlaps the large QTL for hybrid breakdown, indicating that divergence of these species may have occurred due to a complex interplay of ecological divergence and accumulation of intrinsic genetic incompatibilities.     

Ernst Mayr and the integration of geographic and ecological factors in speciation

Mayr's best recognized scientific contributions include the biological species concept and the theory of geographic speciation. In the latter, reproductive isolation evolves as an incidental by‐product of genetic divergence between allopatric populations. Mayr noted that divergent natural selection could accelerate speciation, but also argued that gene flow so strongly retards divergence that, even with selection, non‐allopatric speciation is unlikely. However, current theory and data demonstrate that substantial divergence, and even speciation, in the face of gene flow is possible. Here, I attempt to connect some opposing views about speciation by integrating Mayr's ideas about the roles of ecology and geography in speciation with current data and theory. My central premise is that the speciation process (i.e. divergence) is often continuous, and that the opposing processes of selection and gene flow interact to determine the degree of divergence (i.e. the degree of progress towards the completion of speciation). I first establish that, in the absence of gene flow, divergent selection often promotes speciation. I then discuss how population differentiation in the face of gene flow is common when divergent selection occurs. However, such population differentiation does not always lead to the evolution of discontinuities, strong reproductive isolation, and thus speciation per se. I therefore explore the genetic and ecological circumstances that facilitate speciation in the face of gene flow. For example, particular genetic architectures or ecological niches may tip the balance between selection and gene flow strongly in favour of selection. The circumstances allowing selection to overcome gene flow to the extent that a discontinuity develops, and how often these circumstances occur, are major remaining questions in speciation research. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 26–46.     

Complex trait divergence contributes to environmental niche differentiation in ecological speciation of Boechera stricta

Ecological factors may contribute to reproductive isolation if differential local adaptation causes immigrant or hybrid fitness reduction. Because local adaptation results from the interaction between natural selection and adaptive traits, it is crucial to investigate both to understand ecological speciation. Previously, we used niche modelling to identify local water availability as an environmental correlate of incipient ecological speciation between two subspecies in Boechera stricta, a close relative of Arabidopsis. Here, we performed several large‐scale glasshouse experiments to investigate the divergence of various physiological, phenological and morphological traits. Although we found no significant difference in physiological traits, the Western subspecies has significantly faster growth rate, larger leaf area, less succulent leaves, delayed reproductive time and longer flowering duration. These trait differences are concordant with previous results that habitats of the Western genotypes have more consistent water availability, while Eastern genotypes inhabit locations with more ephemeral water supplies. In addition, by comparing univariate and multivariate divergence of complex traits (Q_ST) to the genomewide distribution of SNP F_ST, we conclude that the aspects of phenology and morphology (but not physiology) are under divergent selection. In addition, we also identified several highly diverged traits without obvious water‐related functions.