GENETIC DISTANCE BETWEEN SPECIES PREDICTS NOVEL TRAIT EXPRESSION IN THEIR HYBRIDS

Interspecific hybridization can generate transgressive hybrid phenotypes with extreme trait values exceeding the combined range of the parental species. Such variation can enlarge the working surface for natural selection, and may facilitate the evolution of novel adaptations where ecological opportunity exists. The number of quantitative trait loci fixed for different alleles in different species should increase with time since speciation. If transgression is caused by complementary gene action or epistasis, hybrids between more distant species should be more likely to display transgressive phenotypes. To test this prediction we collected data on transgression frequency from the literature, estimated genetic distances between the hybridizing species from gene sequences, and calculated the relationship between the two using phylogenetically controlled methods. We also tested if parental phenotypic divergence affected the occurrence of transgression. We found a highly significant positive correlation between transgression frequency and genetic distance in eudicot plants explaining 43% of the variance in transgression frequency. In total, 36% of the measured traits were transgressive. The predicted effect of time since speciation on transgressive segregation was unconfounded by the potentially conflicting effects of phenotypic differentiation between species. Our analysis demonstrates that the potential impact hybridization may have on phenotypic evolution is predictable from the genetic distance between species.     

Weak disruptive selection and incomplete phenotypic divergence in two classic examples of sympatric speciation: cameroon crater lake cichlids

Abstract Recent documentation of a few compelling examples of sympatric speciation led to a proliferation of theoretical models. Unfortunately, plausible examples from nature have rarely been used to test model predictions, such as the initial presence of strong disruptive selection. Here I estimated the form and strength of selection in two classic examples of sympatric speciation: radiations of Cameroon cichlids restricted to Lakes Barombi Mbo and Ejagham. I measured five functional traits and relative growth rates in over 500 individuals within incipient species complexes from each lake. Disruptive selection was prevalent in both groups on single and multivariate trait axes but weak relative to stabilizing selection on other traits and most published estimates of disruptive selection. Furthermore, despite genetic structure, assortative mating, and bimodal species-diagnostic coloration, trait distributions were unimodal in both species complexes, indicating the earliest stages of speciation. Long waiting times or incomplete sympatric speciation may result when disruptive selection is initially weak. Alternatively, I present evidence of additional constraints in both species complexes, including weak linkage between coloration and morphology, reduced morphological variance aligned with nonlinear selection surfaces, and minimal ecological divergence. While other species within these radiations show complete phenotypic separation, morphological and ecological divergence in these species complexes may be slow or incomplete outside optimal parameter ranges, in contrast to rapid divergence of their sexual coloration.     

Positive correlation between diversification rates and phenotypic evolvability can mimic punctuated equilibrium on molecular phylogenies

The hypothesis of punctuated equilibrium proposes that most phenotypic evolution occurs in rapid bursts associated with speciation events. Several methods have been developed that can infer punctuated equilibrium from molecular phylogenies in the absence of paleontological data. These methods essentially test whether the variance in phenotypes among extant species is better explained by evolutionary time since common ancestry or by the number of estimated speciation events separating taxa. However, apparent "punctuational" trait change can be recovered on molecular phylogenies if the rate of phenotypic evolution is correlated with the rate of speciation. Strong support for punctuational models can arise even if the underlying mode of trait evolution is strictly gradual, so long as rates of speciation and trait evolution covary across the branches of phylogenetic trees, and provided that lineages vary in their rate of speciation. Species selection for accelerated rates of ecological or phenotypic divergence can potentially lead to the perception that most trait divergence occurs in association with speciation events.     

Crossing relationships among ancient and experimental sunflower hybrid lineages

Abstract.— Reproductive barrier formation between newly derived hybrid taxa and their parental species represents a major evolutionary hurdle. Here, I examine the development of a sterility barrier during hybrid speciation by examining the fertility of progeny from all combinations of crosses involving three experimentally synthesized sunflower hybrid lineages, their natural hybrid counterpart, Helianthus anomalus , and their parents, H. annuus and H. petiolaris . Crosses between the parental species and H. anomalus generated almost completely sterile offspring (pollen viability < 5%; seed set < 1%). A fairly strong sterility barrier also has developed between three hybrid lineages and both parental species (pollen viability 11.1–41.6%; seed set 0.84–20.1%). In contrast, the three hybrid lineages are almost fully interfertile (pollen viabilities 83.1–88.6%; seed set 72.1–75.3%), as predicted by molecular mapping studies that indicate they have converged on a similar set of gene combinations and chromosomal rearrangements. A modest decline in compability is observed in crosses between the three hybrid lineages and H. anomalus (pollen viabilities 64.1–70.7%; seed set 37–43%), a result that agrees well with prior data demonstrating significant congruence between the genomes of the natural and experimental hybrid lineages. These observations not only indicate that reproductive isolation can arise as a by-product of fertility selection in hybrid populations, but also testify to the repeatability of this mode of speciation.     

Adaptive speciation when assortative mating is based on female preference for male marker traits

Adaptive speciation occurs when frequency-dependent ecological interactions generate conditions of disruptive selection to which lineage splitting is an adaptive response. Under such selective conditions, evolution of assortative mating mechanisms enables the break-up of the ancestral lineage into diverging and reproductively isolated descendent species. Extending previous studies, I investigate models of adaptive speciation due to the evolution of indirect assortative mating that is based on three different mating traits: the degree of assortativity, a female preference trait and a male marker trait. For speciation to occur, linkage disequilibria between different mating traits, e.g. between female preference and male marker traits, as well as between mating traits and the ecological trait, must evolve. This can lead to novel speciation scenarios, e.g. when reproductive isolation is generated by a splitting in the degree of assortativeness, with one of the emerging lineages mating assortatively, and the other one disassortatively. I investigate the effects of variation in various model parameters on the likelihood of speciation, as well as robustness of speciation to introducing costs of assortative mating. Even though in the models presented speciation requires the genetic potential for strong assortment as well as rather restrictive ecological conditions, the results show that adaptive speciation due to the evolution of assortative mating when mate choice is based on separate female preference and male marker traits is a theoretically plausible evolutionary scenario.     

Genetic mapping in hybrid zones

Recent advances in genetic mapping methodologies make it feasible to localize quantitative trait loci (QTL) that contribute to adaptation and speciation. However, it has not been possible to employ these methods in many wild species because of difficulties associated with creating and propagating recombinant populations of sufficient size for QTL mapping. Natural hybrid zones contain recombinant individuals resulting from many generations of hybridization and thus offer a potential solution to these problems. For studies of speciation, hybrid zones offer the possibility of mapping QTL simultaneously with assessments of their effects on assortative mating, hybrid fitness, and interspecific gene flow. Here, we explore the problems and prospects associated with genetic map building and QTL analyses in natural hybrid zones by analyzing correlations among markers of known genomic location in four hybrid zones between the wild sunflower species Helianthus annuus and Helianthus petiolaris. Results indicate that mapping in hybrid zones presents many challenges. These include overlap in the strength of marker correlations between linked and unlinked markers, unevenness in marker frequencies along linkages, and heterogeneity in the relationship between marker distances and correlations. All make it difficult to accurately group and order markers or to estimate the distances between them. These problems can be ameliorated by sampling strategies that maximize the difference in linkage disequilibria between linked and unlinked markers and that minimize differences in frequencies among markers or QTL. In addition, studies that employ a previously determined molecular marker map for gene localization have a greater likelihood of success than those that rely on the hybrid zone data for both map construction and QTL analyses.     

The ecological genetics of homoploid hybrid speciation

Our understanding of homoploid hybrid speciation has advanced substantially since this mechanism of species formation was codified 50 years ago. Early theory and research focused almost exclusively on the importance of chromosomal rearrangements, but it later became evident that natural selection, specifically ecological selection, might play a major role as well. In light of this recent shift, we present an evaluation of ecology's role in homoploid hybrid speciation, with an emphasis on the genetics underlying ecological components of the speciation process. We briefly review new theoretical developments related to the ecology of homoploid hybrid speciation; propose a set of explicit, testable questions that must be answered to verify the role of ecological selection in homoploid hybrid speciation; discuss published work with reference to these questions; and also report new data supporting the importance of ecological selection in the origin of the homoploid hybrid sunflower species Helianthus deserticola. Overall, theory and empirical evidence gathered to date suggest that ecological selection is a major factor promoting homoploid hybrid speciation, with the strongest evidence coming from genetic studies.     

Ambiguous species boundaries: Hybridization and morphological variation in two closely related Rubus species along altitudinal gradients

Although hybridization frequently occurs among plant species, hybrid zones of divergent lineages formed at species boundaries are less common and may not be apparent in later generations of hybrids with more parental‐like phenotypes, as a consequence of backcrossing. To determine the effects of dispersal and selection on species boundaries, we compared clines in leaf traits and molecular hybrid index along two hybrid zones on Yakushima Island, Japan, in which a temperate (Rubus palmatus) and subtropical (Rubus grayanus) species of wild raspberry are found. Leaf sinus depth in the two hybrid zones had narrower clines at 600 m a.s.l. than the molecular hybrid index and common garden tests confirmed that some leaf traits, including leaf sinus depth that is a major trait used in species identification, are genetically divergent between these closely related species. The sharp transition in leaf phenotypic traits compared to molecular markers indicated divergent selection pressure on the hybrid zone structure. We suggest that species boundaries based on neutral molecular data may differ from those based on observed morphological traits.     

Disruptive ecological selection on a mating cue

Adaptation to divergent ecological niches can result in speciation. Traits subject to disruptive selection that also contribute to non-random mating will facilitate speciation with gene flow. Such ‘magic’ or ‘multiple-effect’ traits may be widespread and important for generating biodiversity, but strong empirical evidence is still lacking. Although there is evidence that putative ecological traits are indeed involved in assortative mating, evidence that these same traits are under divergent selection is considerably weaker. Heliconius butterfly wing patterns are subject to positive frequency-dependent selection by predators, owing to aposematism and Müllerian mimicry, and divergent colour patterns are used by closely related species to recognize potential mates. The amenability of colour patterns to experimental manipulation, independent of other traits, presents an excellent opportunity to test their role during speciation. We conducted field experiments with artificial butterflies, designed to match natural butterflies with respect to avian vision. These were complemented with enclosure trials with live birds and real butterflies. Our experiments showed that hybrid colour-pattern phenotypes are attacked more frequently than parental forms. For the first time, we demonstrate disruptive ecological selection on a trait that also acts as a mating cue.     

Changes in sexual signals are greater than changes in ecological traits in a dichromatic group of fishes

Understanding the mechanisms by which phenotypic divergence occurs is central to speciation research. These mechanisms can be revealed by measuring differences in traits that are subject to different selection pressures; greater influence of different types of selection can be inferred from greater divergence in associated traits. Here, we address the potential roles of natural and sexual selection in promoting phenotypic divergence between species of snubnose darters by comparing differences in body shape, an ecologically relevant trait, and male color, a sexual signal. Body shape was measured using geometric morphometrics, and male color was measured using digital photography and visual system‐dependent color values. Differences in male color are larger than differences in body shape across eight allopatric, phylogenetically independent species pairs. While this does not exclude the action of divergent natural selection, our results suggest a relatively more important role for sexual selection in promoting recent divergence in darters. Variation in the relative differences between male color and body shape across species pairs reflects the continuous nature of speciation mechanisms, ranging from ecological speciation to speciation by sexual selection alone.     

Evolution of mate choice and the so‐called magic traits in ecological speciation

Non‐random mating provides multiple evolutionary benefits and can result in speciation. Biological organisms are characterised by a myriad of different traits, many of which can serve as mating cues. We consider multiple mechanisms of non‐random mating simultaneously within a unified modelling framework in an attempt to understand better which are more likely to evolve in natural populations going through the process of local adaptation and ecological speciation. We show that certain traits that are under direct natural selection are more likely to be co‐opted as mating cues, leading to the appearance of magic traits (i.e. phenotypic traits involved in both local adaptation and mating decisions). Multiple mechanisms of non‐random mating can interact so that trait co‐evolution enables the evolution of non‐random mating mechanisms that would not evolve alone. The presence of magic traits may suggest that ecological selection was acting during the origin of new species.     

Genome-wide patterns of divergence during speciation: the lake whitefish case study

The nature, size and distribution of the genomic regions underlying divergence and promoting reproductive isolation remain largely unknown. Here, we summarize ongoing efforts using young (12 000 yr BP) species pairs of lake whitefish (Coregonus clupeaformis) to expand our understanding of the initial genomic patterns of divergence observed during speciation. Our results confirmed the predictions that: (i) on average, phenotypic quantitative trait loci (pQTL) show higher F(ST) values and are more likely to be outliers (and therefore candidates for being targets of divergent selection) than non-pQTL markers; (ii) large islands of divergence rather than small independent regions under selection characterize the early stages of adaptive divergence of lake whitefish; and (iii) there is a general trend towards an increase in terms of numbers and size of genomic regions of divergence from the least (East L.) to the most differentiated species pair (Cliff L.). This is consistent with previous estimates of reproductive isolation between these species pairs being driven by the same selective forces responsible for environment specialization. Altogether, dwarf and normal whitefish species pairs represent a continuum of both morphological and genomic differentiation contributing to ecological speciation. Admittedly, much progress is still required to more finely map and circumscribe genomic islands of speciation. This will be achieved through the use of next generation sequencing data but also through a better quantification of phenotypic traits moulded by selection as organisms adapt to new environmental conditions.     

Divergent sexual selection via male competition: ecology is key

Sexual selection and ecological differences are important drivers of speciation. Much research has focused on female choice, yet the role of male competition in ecological speciation has been understudied. Here, we test how mating habitats impact sexual selection and speciation through male competition. Using limnetic and benthic species of threespine stickleback fish, we find that different mating habitats select differently on male traits through male competition. In mixed habitat with both vegetated and open areas, selection favours two trait combinations of male body size and nuptial colour: large with little colour and small with lots of colour. This matches what we see in reproductively isolated stickleback species, suggesting male competition could promote trait divergence and reproductive isolation. In contrast, when only open habitat exists, selection favours one trait combination, large with lots of colour, which would hinder trait divergence and reproductive isolation. Other behavioural mechanisms in male competition that might promote divergence, such as avoiding aggression with heterospecifics, are insufficient to maintain separate species. This work highlights the importance of mating habitats in male competition for both sexual selection and speciation.     

Remarkable life history polymorphism may be evolving under divergent selection in the silverleaf sunflower

Substantial intraspecific variation in life history is rare and potentially a signal of incipient ecological speciation, if variation is driven by geographically heterogenous natural selection. We present the first report of extensive life history polymorphism in Helianthus argophyllus, the silverleaf sunflower, and examine evidence for its evolution by divergent selection. In 18 populations sampled from across the species range and grown in a common garden, most quantitative traits covaried such that individuals could be assigned to two distinct life history syndromes: tall and late flowering with small initial flowerheads, or short and early flowering with larger initial flowerheads. Helianthus argophyllus exhibits regional genetic structure, but this population structure does not closely correspond with patterns of phenotypic variation. The early‐flowering syndrome is primarily observed in populations from coastal barrier islands, while populations from the nearby mainland coast, although geographically and genetically close, are primarily late flowering. Additionally, several traits are more differentiated among regions than expected based on neutral genetic divergence (Q_ST > F_ST), including the first principal component score corresponding with life history syndrome. This discordance between patterns of phenotypic and genetic variation suggests that divergent selection is driving genetic differences in life history across the species range. If so, the silverleaf sunflower may be in early stages of ecological speciation.     

A quantitative genetic analysis of male sexual traits distinguishing the sibling species Drosophila simulans and D. sechellia

A quantitative trait locus (QTL) genetic analysis of morphological and reproductive traits distinguishing the sibling species Drosophila simulans and D. sechellia was carried out in a backcross design, using 38 markers with an average spacing of 8.4 cM. The direction of QTL effects for the size of the posterior lobe was consistent across the identified QTL, indicating directional selection for this trait. Directional selection also appears to have acted on testis length, indicating that sexual selection may have influenced many reproductive traits, although other forms of directional selection cannot be ruled out. Sex comb tooth number exhibited high levels of variation both within and among isofemale lines and showed no evidence for directional selection and, therefore, may not have been involved in the early speciation process. A database search for genes associated with significant QTL revealed a set of candidate loci for posterior lobe shape and size, sex comb tooth number, testis length, tibia length, and hybrid male fertility. In particular, decapentaplegic (dpp), a gene known to influence the genital arch, was found to be associated with the largest LOD peak for posterior lobe shape and size.     

Molecular genetic and quantitative trait divergence associated with recent homoploid hybrid speciation: a study of Senecio squalidus (Asteraceae)

Hybridization is increasingly seen as a trigger for rapid evolution and speciation. To quantify and qualify divergence associated with recent homoploid hybrid speciation, we compared quantitative trait (QT) and molecular genetic variation between the homoploid hybrid species Senecio squalidus and its parental species, S. aethnensis and S. chrysanthemifolius, and also their naturally occurring Sicilian hybrids. S. squalidus originated and became invasive in the United Kingdom following the introduction of hybrid plants from Mount Etna, Sicily, about 300 years ago. We recorded considerable molecular genetic differentiation between S. squalidus and its parents and their Sicilian hybrids in terms of both reduced genetic diversity and altered allele frequencies, potentially due to the genetic bottleneck associated with introduction to the United Kingdom. S. squalidus is also distinct from its parents and Sicilian hybrids for QTs, but less so than for molecular genetic markers. We suggest that this is due to resilience of polygenic QTs to changes in allele frequency or lack of selection for hybrid niche divergence in geographic isolation. While S. squalidus is intermediate or parental-like for most QTs, some trangressively distinct traits were observed, which might indicate emerging local adaptation in its invasive range. This study emphasizes the important contribution of founder events and geographic isolation to successful homoploid hybrid speciation.     

Sexual dimorphism and adaptive speciation: two sides of the same ecological coin

Models of adaptive speciation are typically concerned with demonstrating that it is possible for ecologically driven disruptive selection to lead to the evolution of assortative mating and hence speciation. However, disruptive selection could also lead to other forms of evolutionary diversification, including ecological sexual dimorphisms. Using a model of frequency-dependent intraspecific competition, we show analytically that adaptive speciation and dimorphism require identical ecological conditions. Numerical simulations of individual-based models show that a single ecological model can produce either evolutionary outcome, depending on the genetic independence of male and female traits and the potential strength of assortative mating. Speciation is inhibited when the genetic basis of male and female ecological traits allows the sexes to diverge substantially. This is because sexual dimorphism, which can evolve quickly, can eliminate the frequency-dependent disruptive selection that would have provided the impetus for speciation. Conversely, populations with strong assortative mating based on ecological traits are less likely to evolve a sexual dimorphism because females cannot simultaneously prefer males more similar to themselves while still allowing the males to diverge. This conflict between speciation and dimorphism can be circumvented in two ways. First, we find a novel form of speciation via negative assortative mating, leading to two dimorphic daughter species. Second, if assortative mating is based on a neutral marker trait, trophic dimorphism and speciation by positive assortative mating can occur simultaneously. We conclude that while adaptive speciation and ecological sexual dimorphism may occur simultaneously, allowing for sexual dimorphism restricts the likelihood of adaptive speciation. Thus, it is important to recognize that disruptive selection due to frequency-dependent interactions can lead to more than one form of adaptive splitting.     

Inferring speciation modes in a clade of Iberian chafers from rates of morphological evolution in different character systems

Background  

Studies of speciation mode based on phylogenies usually test the predicted effect on diversification patterns or on geographical distribution of closely related species. Here we outline an approach to infer the prevalent speciation mode in Iberian Hymenoplia chafers through the comparison of the evolutionary rates of morphological character systems likely to be related to sexual or ecological selection. Assuming that mitochondrial evolution is neutral and not related to measured phenotypic differences among the species, we contrast hypothetic outcomes of three speciation modes: 1) geographic isolation with subsequent random morphological divergence, resulting in overall change proportional to the mtDNA rate; 2) sexual selection on size and shape of the male intromittent organs, resulting in an evolutionary rate decoupled to that of the mtDNA; and 3) ecological segregation, reflected in character systems presumably related to ecological or biological adaptations, with rates decoupled from that of the mtDNA.     

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.     

Influences of gene flow on adaptive speciation in the Dubautia arborea--D. ciliolata complex

Mechanisms of reproductive isolation during plant speciation are often unclear because distinct species often experience high levels of gene flow and hybridization. Adaptive radiations such as the Hawaiian silversword alliance (HSA) provide unique opportunities to study the interactions of selection, gene flow and isolating mechanisms during the speciation process. We examined patterns of phenotypic and genetic differentiation in Dubautia arborea and Dubautia ciliolata, two parapatric HSA taxa that show marked morphological divergence but evidence of weak molecular differentiation, in order to estimate genome-wide differentiation and gene flow patterns. We scored 166 amplified fragment length polymorphism markers in a set of 89 plants from two populations each of D. arborea and D. ciliolata and phenotypically D. arborea-like and D. ciliolata-like plants from a natural hybrid zone. Analyses of population subdivision showed low levels of differentiation between the two species (F(ST) = 0.089) and evidence that the phenotypically parental hybrid zone plants were largely of parental species rather than of hybrid origin. A Bayesian analysis of population ancestry identified a number of plants with admixed D. arborea and D. ciliolata ancestry, even in nonhybrid-zone populations. These results suggest that genome-wide low levels of differentiation between D. arborea and D. ciliolata are in part due to gene flow, and favour models of genic speciation and collective evolution in which gene flow has different effects on selected loci vs. nonselected genomic regions. We discuss ecological and climatic factors that may have shaped patterns of differentiation in this species complex.