Evolution Of Reproductive Isolation Research Articles

Morphologically cryptic Amazonian bird species pairs exhibit strong postzygotic reproductive isolation.

We possess limited understanding of how speciation unfolds in the most species-rich region of the planet-the Amazon basin. Hybrid zones provide valuable information on the evolution of reproductive isolation, but few studies of Amazonian vertebrate hybrid zones have rigorously examined the genome-wide underpinnings of reproductive isolation. We used genome-wide genetic datasets to show that two deeply diverged, but morphologically cryptic sister species of forest understorey birds show little evidence for prezygotic reproductive isolation, but substantial postzygotic isolation. Patterns of heterozygosity and hybrid index revealed that hybrid classes with heavily recombined genomes are rare and closely match simulations with high levels of selection against hybrids. Genomic and geographical clines exhibit a remarkable similarity across loci in cline centres, and have exceptionally narrow cline widths, suggesting that postzygotic isolation is driven by genetic incompatibilities at many loci, rather than a few loci of strong effect. We propose Amazonian understorey forest birds speciate slowly via gradual accumulation of postzygotic genetic incompatibilities, with prezygotic barriers playing a less important role. Our results suggest old, cryptic Amazonian taxa classified as subspecies could have substantial postzygotic isolation deserving species recognition and that species richness is likely to be substantially underestimated in Amazonia.

Niche divergence along a fine‐scale ecological gradient in sympatric color morphs of a coral reef fish

AbstractColor polymorphisms offer unique opportunities for testing the role of ecological adaptation and natural selection in the origin of species. However, the ecological conditions that facilitate the coexistence and speciation of color morphs in nature remain poorly understood. In this study, we investigate the ecological mechanisms maintaining the color polymorphism in the arc‐eye hawkfish (Paracirrhites arcatus), which consists of two common morphs (pink white‐striped [PWS] and melanistic [MEL]) and less common intermediates that all coexist on shallow coral reefs throughout the Indo‐Pacific. Our approach was to test whether ecologically based disruptive selection on color could explain the maintenance of and possible incipient divergence between sympatric color morphs. We compared patterns of spatial distribution, abundance, habitat use and preference, and niche overlap among color morphs at nine sites along the leeward coast of Hawaii Island. We demonstrate that despite co‐occurring at all sites, sympatric color morphs show significant niche divergence along a steep ecological gradient. Morph frequencies correlate strongly with a multivariate gradient in coral community and reef topography, which explained 81% of the variability in relative abundance of the two main color morphs. Melanistic morphs were more frequent in shallow, steep surge zones dominated byPocilloporacorals. In contrast, PWS morphs were more frequent in deeper, sub‐surge zones with higher coral cover dominated byPoritescorals. Niche overlap analyses highlight how the two main morphs are partitioned on opposite ends of this continuous ecological gradient, while phenotypic intermediates are mostly restricted to intermediate habitats. The strong correlation between phenotype and environment suggests that morphs have fitness advantages in their respective habitats. We speculate that disruptive natural selection on color pattern to increase crypsis in heterogeneous visual environments has led to divergence in habitat preferences. The resulting ecological isolation provides a plausible mechanism for the persistence of multiple coexisting color phenotypes inP. arcatus. If divergence in color also affects mate choice, the evolution of reproductive isolation is likely to be promoted.

Patterns of genetic variation among geographic and host-plant associated populations of the peach fruit moth Carposina sasakii (Lepidoptera: Carposinidae)

BackgroundPopulations of herbivorous insects may become genetically differentiated because of local adaptation to different hosts and climates as well as historical processes, and further genetic divergence may occur following the development of reproductive isolation among populations. Here we investigate the population genetic structure of the orchard pest peach fruit moth (PFM) Carposina sasakii (Lepidoptera: Carposinidae) in China, which shows distinct biological differences when characterized from different host plants. Genetic diversity and genetic structure were assessed among populations from seven plant hosts and nine regions using 19 microsatellite loci and a mitochondrial sequence.ResultsStrong genetic differentiation was found among geographical populations representing distinct geographical regions, but not in host-associated populations collected from the same area. Mantel tests based on microsatellite loci indicated an association between genetic differentiation and geographical distance, and to a lesser extent environmental differentiation. Approximate Bayesian Computation analyses supported the scenario that PFM likely originated from a southern area and dispersed northwards before the last glacial maximum during the Quaternary.ConclusionsOur analyses suggested a strong impact of geographical barriers and historical events rather than host plants on the genetic structure of the PFM; however, uncharacterized environmental factors and host plants may also play a role. Studies on adaptive shifts in this moth should take into account geographical and historical factors.

Narrow hybrid zones in spite of very low population differentiation in neutral markers in an island bird species complex.

Patterns of phenotypic and genic frequencies across hybrid zones provide insight into the origin and evolution of reproductive isolation. The Reunion grey white-eye, Zosterops borbonicus, exhibits parapatrically distributed plumage colour forms across the lowlands of the small volcanic island of Reunion (Mascarene archipelago). These forms meet and hybridize in regions that are natural barriers to dispersal (rivers, lava fields). Here, we investigated the relationship among patterns of differentiation at neutral genetic (microsatellite) markers, phenotypic traits (morphology and plumage colour) and niche characteristics across three independent hybrid zones. Patterns of phenotypic divergence revealed that these hybrid zones are among the narrowest ever documented in birds. However, the levels of phenotypic divergence stand in stark contrast to the lack of clear population neutral genetic structure between forms. The position of the hybrid zones coincides with different natural physical barriers, yet is not associated with steep changes in vegetation and related climatic variables, and major habitat transitions are shifted from these locations by at least 18km. This suggests that the hybrid zones are stabilized over natural dispersal barriers, independently of environmental boundaries, and are not associated with niche divergence. A striking feature of these hybrid zones is the very low levels of genetic differentiation in neutral markers between forms, suggesting that phenotypic divergence has a narrow genetic basis and may reflect recent divergence at a few linked genes under strong selection, with a possible role for assortative mating in keeping these forms apart.

Hybrid sterility increases with genetic distance in snubnose darters (Percidae: Etheostoma)

The process of speciation is often synonymous with the evolution of reproductive isolation, and the tempo at which reproductive barriers evolve can provide insight into the underlying mechanisms of divergence. Darters are a diverse group of North American freshwater fish in which behavioral isolation appears to evolve rapidly; however, little is known about hybrid sterility among darter species. Here, six allopatric pairs of darter species were hybridized via in vitro fertilization and offspring were reared to reproductive age. Hybrid sterility appears more pronounced in male hybrids. Additionally, levels of hybrid sterility increase with genetic distance across species pairs. Understanding sex determination and sex-specific gene expression in darters will provide further insight into the evolution of hybrid sterility.

The Roles of Sexual and Viability Selection in the Evolution of Incomplete Reproductive Isolation: From Allopatry to Sympatry

In recent years, theoretical models have introduced the concept that ongoing hybridization between "good" species can occur because incomplete reproductive isolation can be a selected optimum. They furthermore show that positive frequency-dependent sexual selection, which is naturally generated by some of the underlying processes that lead to assortative mating, plays a key role in the evolution of incomplete reproductive isolation. This occurs, however, through different mechanisms in sympatric versus allopatric scenarios. We investigate the evolution of incomplete reproductive isolation by sexual selection in scenarios ranging from sympatry to allopatry, to examine how these mechanisms interact. We consider an ecological scenario in which there are two habitats used during foraging and individuals can breed either within a habitat or in a common mating pool. We find that when trait divergence is maintained, sexual selection drives the evolution of choosiness in opposite ways in the common mating pool versus within each habitat. Specifically, strong choosiness is favored in the common mating pool, whereas intermediate choosiness is favored within habitat; the interaction of these forces determines whether intermediate reproductive isolation ultimately evolves in the system. We further find cases where the evolution of stronger choosiness occurs but leads to the loss of divergence. Overall, our study shows that contrasting forces on the evolution of reproductive isolation can occur in different mating areas, and we propose a new avenue for understanding the diversity in levels of reproductive isolation within and across species.

Interpreting the genomic landscape of speciation: a road map for finding barriers to gene flow.

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.

The role of allochrony in speciation.

The importance of sympatric speciation - the evolution of reproductive isolation between codistributed conspecific individuals - in generating biodiversity is highly controversial. Allochrony, or differences in breeding time (phenology) between conspecific individuals, has the potential to lead to reproductive isolation and therefore speciation. We critically review the literature to test the importance of allochronic speciation over the three timescales over which allochrony can occur - over the day, between seasons or between years - and explore what is known about genomic mechanisms underlying allochrony in the diverse taxa in which it is found. We found that allochrony can be a key contributor to reproductive isolation, especially if populations have little overlap in breeding time and therefore little potential for gene flow, and may sometimes be the initial or key driver of speciation. Shifts in phenology can be caused by several factors, including a new ecological opportunity, environmental change, or reinforcement. The underlying genomic basis of allochrony has been studied mostly in insects, highlighting the need for genomic studies in other taxa; nonetheless, results to date indicate that several cases of allochrony involve changes in circadian genes. This review provides the first comprehensive discussion of the role of allochrony in speciation and demonstrates that allochrony as a contributor to divergence may be more widespread than previously thought. Understanding genomic changes and adaptations allowing organisms to breed at new times may be key in the light of phenological changes required under climate change.

Sexual selection, sexual isolation and pheromones in Drosophila melanogaster strains after long-term maintaining on different diets

Evolution of reproductive isolation may be a consequence of a variety of signals used in courtship and mate preferences. Pheromones play an important role in both sexual selection and sexual isolation. The abundance of pheromones in Drosophila melanogaster may depend on different environmental factors, including diet. The aim of this study was to ascertain to which degree principal pheromones affect sexual selection in D. melanogaster. We used D. melanogaster strains reared for 14 years on four substrates: standard cornmeal substrate and those containing tomato, banana and carrot. We have previously determined that long-term maintaining of these dietary strains resulted in differences in their cuticular hydrocarbons profile (CHs). In this work, we have tested the level of sexual selection and sexual isolation between aforementioned strains. We found that the high levels of cis-vaccenyl acetate, 7-pentacosene and 7,11-nonacosadiene in the strain reared on a substrate containing carrot affected the individual attractiveness and influenced sexual isolation between flies of this strain and flies reared on a substrate containing banana. Based on these results, long-term different diets, may contribute, to sexual behaviour of D. melanogaster via the effects of principal pheromones.

Spatial turnover in host-plant availability drives host-associated divergence in a South African leafhopper (Cephalelus uncinatus)

BackgroundThe evolution of reproductive isolation between herbivorous insect populations is often initiated by shifts to novel host-plants, a process that underlies some of the best examples of ecological speciation. However, it is not well understood why host-shifts occur. Arguably the most common hypothesis is that host-shifts occur in response to competition, while a less frequently invoked hypothesis is that herbivores adapt locally to geographic differences in potential host-plant communities. Here we investigate whether geographic variation in host-plant availability is likely to have driven host-shifts in restio leafhoppers. We studied local adaptation of a camouflaged restio leafhopper species, Cephalelus uncinatus, to host-plants in the Restionaceae (restios); a family of plants with exceptional diversity in the anomalously species-rich Cape Floristic Region (CFR). To determine whether C. uncinatus experiences heterogeneous host communities across its range, we first quantified the degree of geographic overlap between C. uncinatus and each of its associated host-plant species. Then we quantified trait divergence (host preference, body size and colour) for three pairs of C. uncinatus populations found on different host-plant species differing in their degree of spatial overlap. Spectral reflectance was modelled in bird visual space to investigate whether body colour divergence in C. uncinatus corresponds to leaf sheath colour differences between restio species as perceived by potential predators.ResultsWe demonstrate that C. uncinatus is forced to use different restio species in different regions because of turnover in available host species across its range. Comparisons between geographically separated populations were consistent with local adaptation: restio leafhoppers had preferences for local host-plants over alternative host-plants and matched local plants better in terms of size and colour.ConclusionsSpatial turnover in host-plant availability has likely facilitated host-shifts in C. uncinatus. Spatial turnover in host-plant availability may be an important driver of insect diversification in the CFR and globally.

Evolution of reproductive isolation in stickleback fish.

To understand how new species form and what causes their collapse, we examined how reproductive isolation evolves during the speciation process, considering species pairs with little to extensive divergence, including a recently collapsed pair. We estimated many reproductive barriers in each of five sets of stickleback fish species pairs using our own data and decades of previous work. We found that the types of barriers important early in the speciation process differ from those important late. Two premating barriers-habitat and sexual isolation-evolve early in divergence and remain two of the strongest barriers throughout speciation. Premating isolation evolves before postmating isolation, and extrinsic isolation is far stronger than intrinsic. Completing speciation, however, may require postmating intrinsic incompatibilities. Reverse speciation in one species pair was characterized by significant loss of sexual isolation. We present estimates of barrier strengths before and after collapse of a species pair; such detail regarding the loss of isolation has never before been documented. Additionally, despite significant asymmetries in individual barriers, which can limit speciation, total isolation was essentially symmetric between species. Our study provides important insight into the order of barrier evolution and the relative importance of isolating barriers during speciation and tests fundamental predictions of ecological speciation.

Divergence of cuticular hydrocarbons in two sympatric grasshopper species and the evolution of fatty acid synthases and elongases across insects.

Cuticular hydrocarbons (CHCs) play a major role in the evolution of reproductive isolation between insect species. The CHC profiles of two closely related sympatric grasshopper species, Chorthippus biguttulus and C. mollis, differ mainly in the position of the first methyl group in major methyl-branched CHCs. The position of methyl branches is determined either by a fatty acid synthase (FAS) or by elongases. Both protein families showed an expansion in insects. Interestingly, the FAS family showed several lineage-specific expansions, especially in insect orders with highly diverse methyl-branched CHC profiles. We found five putative FASs and 12 putative elongases in the reference transcriptomes for both species. A dN/dS test showed no evidence for positive selection acting on FASs and elongases in these grasshoppers. However, one candidate FAS showed species-specific transcriptional differences and may contribute to the shift of the methyl-branch position between the species. In addition, transcript levels of four elongases were expressed differentially between the sexes. Our study indicates that complex methyl-branched CHC profiles are linked to an expansion of FASs genes, but that species differences can also mediated at the transcriptional level.

Genomic landscape of early ecological speciation initiated by selection on nuptial colour.

Ecological speciation is the evolution of reproductive isolation as a consequence of direct divergent natural selection or ecologically mediated divergent sexual selection. While the genomic signature of the former has been extensively studied in recent years, only few examples exist for genomic differentiation where environment-dependent sexual selection has played an important role. Here, we describe a very young (~90years old) population of threespine sticklebacks exhibiting phenotypic and genomic differentiation between two habitats within the same pond. We show that differentiation among habitats is limited to male throat colour and nest type, traits known to be subject to sexual selection. Divergence in these traits mirrors divergence in much older benthic and limnetic stickleback species pairs from North American west coast lakes, which also occur in sympatry but are strongly reproductively isolated from each other. We demonstrate that in our population, differences in throat colour and breeding have been stable over a decade, but in contrast to North American benthic and limnetic stickleback species, these mating trait differences are not accompanied by divergence in morphology related to feeding, predator defence or swimming performance. Using genomewide SNP data, we find multiple genomic islands with moderate differentiation spread across several chromosomes, whereas the rest of the genome is undifferentiated. The islands contain potential candidate genes involved in visual perception of colour. Our results suggest that phenotypic and multichromosome genomic divergence of these morphs was driven by environment-dependent sexual selection, demonstrating incipient speciation after only a few decades of divergence in sympatry.

Population differentiation at a regional scale in spadefoot toads: contributions of distance and divergent selective environments.

The causes of population differentiation can provide insight into the origins of early barriers to gene flow. Two key drivers of population differentiation are geographic distance and local adaptation to divergent selective environments. When reproductive isolation arises because some populations of a species are under selection to avoid hybridization while others are not, population differentiation and even speciation can result. Spadefoot toad populations Spea multiplicata that are sympatric with a congener have undergone reinforcement. This reinforcement has resulted not only in increased reproductive isolation from the congener, but also in the evolution of reproductive isolation from nearby and distant conspecific allopatric populations. We used multiple approaches to evaluate the contributions of geographic distance and divergent selective environments to population structure across this regional scale in S. multiplicata, based on genotypes from six nuclear microsatellite markers. We compared groups of populations varying in both geographic location and in the presence of a congener. Hierarchical F-statistics and results from cluster analyses and discriminant analyses of principal components all indicate that geographic distance is the stronger contributor to genetic differentiation among S. multiplicata populations at a regional scale. However, we found evidence that adaptation to divergent selective environments also contributes to population structure. Our findings highlight how variation in the balance of evolutionary forces acting across a species’ range can lead to variation in the relative contributions of geographic distance and local adaptation to population differentiation across different spatial scales.

Postmating-prezygotic isolation between two allopatric populations of Drosophila montana: fertilisation success differs under sperm competition.

Postmating but prezygotic (PMPZ) interactions are increasingly recognized as a potentially important early‐stage barrier in the evolution of reproductive isolation. A recent study described a potential example between populations of the same species: single matings between Drosophila montana populations resulted in differential fertilisation success because of the inability of sperm from one population (Vancouver) to penetrate the eggs of the other population (Colorado). As the natural mating system of D. montana is polyandrous (females remate rapidly), we set up double matings of all possible crosses between the same populations to test whether competitive effects between ejaculates influence this PMPZ isolation. We measured premating isolation in no‐choice tests, female fecundity, fertility and egg‐to‐adult viability after single and double matings as well as second‐male paternity success (P2). Surprisingly, we found no PMPZ reproductive isolation between the two populations under a competitive setting, indicating no difficulty of sperm from Vancouver males to fertilize Colorado eggs after double matings. While there were subtle differences in how P2 changed over time, suggesting that Vancouver males’ sperm are somewhat less competitive in a first‐male role within Colorado females, these effects did not translate into differences in overall P2. Fertilisation success can thus differ dramatically between competitive and noncompetitive conditions, perhaps because the males that mate second produce higher quality ejaculates in response to sperm competition. We suggest that unlike in more divergent species comparisons, where sperm competition typically increases reproductive isolation, ejaculate tailoring can reduce the potential for PMPZ isolation when recently diverged populations interbreed.

Male behaviour predicts trait divergence and the evolution of reproductive isolation in darters (Percidae: Etheostoma)

The diversity of secondary sexual signals across animals has led evolutionary biologists to hypothesize an important role for sexual selection in the process of speciation. Testing this hypothesis typically focuses on male–female mating interactions and divergence in female mate preferences between populations, leading to behavioural reproductive isolation. While informative, these tests rarely account for the potential contributions of male–male competitive interactions and male mate preferences to speciation. By incorporating male and female behavioural data across a genus of colourful freshwater fishes (Percidae: Etheostoma), our results suggest coevolution between male signals and aggressive responses and a potential role for male mating biases alongside female mating biases in the evolution of behavioural isolation between allopatric species. These surprising results imply an important function for male behaviours in trait divergence and the evolution of reproductive isolation, suggesting that a broader view of sexual selection is vital to addressing its role in speciation.

Reduced genetic diversity and increased reproductive isolation follow population-level loss of larval dispersal in a marine gastropod.

Population-level consequences of dispersal ability remain poorly understood, especially for marine animals in which dispersal is typically considered a species-level trait governed by oceanographic transport of microscopic larvae. Transitions from dispersive (planktotrophic) to nondispersive, aplanktonic larvae are predicted to reduce connectivity, genetic diversity within populations, and the spatial scale at which reproductive isolation evolves. However, larval dimorphism within a species is rare, precluding population-level tests. We show the sea slug Costasiella ocellifera expresses both larval morphs in Florida and the Caribbean, regions with divergent mitochondrial lineages. Planktotrophy predominated at 11 sites, 10 of which formed a highly connected and genetically diverse Caribbean metapopulation. Four populations expressed mainly aplanktonic development and had markedly reduced connectivity, and lower genetic diversity at one mitochondrial and six nuclear loci. Aplanktonic dams showed partial postzygotic isolation in most interpopulation crosses, regardless of genetic or geographic distance to the sire's source, suggesting that outbreeding depression affects fragmented populations. Dams from genetically isolated and neighboring populations also exhibited premating isolation, consistent with reinforcement contingent on historical interaction. By increasing self-recruitment and genetic drift, the loss of dispersal may thus initiate a feedback loop resulting in the evolution of reproductive isolation over small spatial scales in the sea.

Testing for parallel allochronic isolation in lake-stream stickleback.

The evolution of reproductive isolation (RI) is a critical step shaping progress towards speciation. In the context of ecological speciation, a critical question is the extent to which specific reproductive barriers important to RI evolve rapidly and predictably in response to environmental differences. Only reproductive barriers with these properties (importance, rapidity, predictability) will drive the diversification of species that are cohesively structured by environment type. One candidate barrier that might exhibit such properties is allochrony, whereby populations breed at different times. We studied six independent lake-stream population pairs of threespine stickleback (Gasterosteus aculeatus Linnaeus, 1758) that are known from genetic studies to show RI. However, the specific reproductive barriers driving this RI have proven elusive, leading to a 'conundrum of missing reproductive isolation'. We here show that breeding times differ among some of the populations, but not in a consistent manner between lakes and streams. Moreover, the timing differences between lake and stream populations within each pair could account for only a small proportion of total RI measured with neutral genetic markers. Allochrony cannot solve the conundrum of missing reproductive isolation in lake-stream stickleback.

Geography, assortative mating, and the effects of sexual selection on speciation with gene flow.

Theoretical and empirical research on the evolution of reproductive isolation have both indicated that the effects of sexual selection on speciation with gene flow are quite complex. As part of this special issue on the contributions of women to basic and applied evolutionary biology, I discuss my work on this question in the context of a broader assessment of the patterns of sexual selection that lead to, versus inhibit, the speciation process, as derived from theoretical research. In particular, I focus on how two factors, the geographic context of speciation and the mechanism leading to assortative mating, interact to alter the effect that sexual selection through mate choice has on speciation. I concentrate on two geographic contexts: sympatry and secondary contact between two geographically separated populations that are exchanging migrants and two mechanisms of assortative mating: phenotype matching and separate preferences and traits. I show that both of these factors must be considered for the effects of sexual selection on speciation to be inferred.

An Integrated Framework for Hybrid Zone Models

Hybridization, where distinguishable populations meet and interbreed resulting in hybrid offspring, is useful for understanding the mechanisms involved in the evolution of reproductive isolation. Hybridization can range from interactions with near-complete reproductive isolation, to stable zones, to complete intergradation. Several models explain how stable hybrid zones are maintained, but each model emphasizes a special case and some zones fit more than one model. The models also do not emphasize moving hybrid zones or occasional hybridization events that add genetic variation to the parental populations. This essay unifies the current models along a continuum of selection pressures organized by geography. Current models differ in assumed hybrid fitness and whether selection is intrinsic or extrinsic. The type of selection is a less general category than the direction of selection (for or against hybrids); multiple types of selection can exist in each zone depending on trait. Thus, the diversity and combinations of selection types make selection direction the most general category for sorting hybrid zones, and variation in selection over geography shapes the spatial extent (in concert with dispersal), movement, and stability of a hybrid zone. This framework is useful for considering zone structure both at the whole organism level and at individual genes or traits. Unifying hybrid zones models by the geographic range of selection pressure organizes each zone into context along the continuum regardless of its fit within one of the classic models, helping us explicitly consider what assumptions are made about the zone and providing direction for further research.