Isolation In Sympatry Research Articles

Testing the predictions of reinforcement: long-term empirical data from a damselfly mottled hybrid zone.

Theoretical work suggests that reinforcement can cause the strengthening of prezygotic isolation in sympatry by mitigating the costs of maladaptive hybridization. However, only a handful of studies have simultaneously tested multiple predictions of this theory in natural populations. We investigated reinforcement in a mottled hybrid zone between the damselflies Ischnura elegans and I. graellsii, which are characterized by incomplete and asymmetric reproductive isolation and exhibit reproductive character displacement in mating-related structures. We tested the conditions for reinforcement by quantifying whether hybridization was costly and prezygotic isolation stronger in sympatry compared with allopatry. Additionally, we investigated two specific predictions of reinforcement: i) greater premating asymmetries in sympatry; and ii) weaker postzygotic isolation in sympatry than in allopatry. Our findings indicate the presence of maladaptive hybrids, which suggests Bateson-Dobzhansky-Müller incompatibilities in allopatry. We also found that reinforcement has strengthened mechanical isolation, at least in one direction in sympatry. We observed evidence for greater premating asymmetries in sympatry than in allopatry, which is consistent with reinforcement. However, fully testing the prediction of weaker postzygotic isolation in sympatry compared to allopatry was hindered by the highly asymmetrical levels of reproductive isolation between the two reciprocal cross directions. Our study highlights a case where reinforcement and heterospecific gene flow exert opposite effects on reproductive isolation between reciprocal crosses, where reinforcement increases reproductive isolation in one direction while gene flow weakens it in the opposite direction.

Acoustic differentiation of calls in the closely related Dartford (Curruca undata), Marmora’s (Curruca sarda) and Balearic Warblers (Curruca balearica)

ABSTRACT Acoustic differentiation in bird vocalisations is a key process for speciation. Calls have received little attention compared to songs, but their simplicity facilitates analysis using mathematical, non-biased, tools, as they can be described by means of very basic variables. Here, we combined PERMANOVA and machine learning techniques to analyse the differentiation in the contact calls of the closely related Dartford (Curruca undata), Marmora’s (C. sarda) and Balearic (C. balearica) warblers (formerly in the genus Sylvia). The calls of the three species differed clearly, consistent with phylogenetic reconstructions based on DNA sequences. In C. sarda, significant call differences were observed between the population wintering in Tunisia (migratory) and those of Sardinia and Corsica (mainly sedentary). Such divergence could be favoured by assortative mating of migrant and resident individuals, working as a matching mechanism for reproductive isolation in sympatry. In contrast, there was no clear separation between the accepted subspecies of C. undata. We found, however, significant differences between the Atlantic and Mediterranean biogeographical regions in this species. The divergences detected within C. undata and C. sarda deserve further investigation, using additional traits to elucidate the phylogenetic status of these groups, as well as the factors driving their diversification.

How Important Is Sexual Isolation to Speciation?

A central role for sexual isolation in the formation of new species and establishment of species boundaries has been noticed since Darwin and is frequently emphasized in the modern literature on speciation. However, an objective evaluation of when and how sexual isolation plays a role in speciation has been carried out in few taxa. We discuss three approaches for assessing the importance of sexual isolation relative to other reproductive barriers, including the relative evolutionary rate of sexual trait differentiation, the relative strength of sexual isolation in sympatry, and the role of sexual isolation in the long-term persistence of diverging forms. First, we evaluate evidence as to whether sexual isolation evolves faster than other reproductive barriers during the early stages of divergence. Second, we discuss available evidence as to whether sexual isolation is as strong or stronger than other barriers between closely related sympatric species. Finally, we consider the effect of sexual isolation on long-term species persistence, relative to other reproductive barriers. We highlight challenges to our knowledge of and opportunities to improve upon our understanding of sexual isolation from different phases of the speciation process.

Despite genetic isolation in sympatry, post-copulatory reproductive barriers have not evolved between bat- and human-associated common bedbugs (Cimex lectularius L.)

BackgroundThe common bedbug Cimex lectularius is a widespread ectoparasite on humans and bats. Two genetically isolated lineages, parasitizing either human (HL) or bat (BL) hosts, have been suggested to differentiate because of their distinct ecology. The distribution range of BL is within that of HL and bedbugs live mostly on synanthropic bat hosts. This sympatric co-occurrence predicts strong reproductive isolation at the post-copulatory level.ResultsWe tested the post-copulatory barrier in three BL and three HL populations in reciprocal crosses, using a common-garden blood diet that was novel to both lineages. We excluded pre-copulation isolation mechanisms and studied egg-laying rates after a single mating until the depletion of sperm, and the fitness of the resulting offspring. We found a higher sperm storage capability in BL, likely reflecting the different seasonal availability of HL and BL hosts. We also observed a notable variation in sperm function at the population level within lineages and significant differences in fecundity and offspring fitness between lineages. However, no difference in egg numbers or offspring fitness was observed between within- and between-lineage crosses.ConclusionsDifferences in sperm storage or egg-laying rates between HL and BL that we found did not affect reproductive isolation. Neither did the population-specific variation in sperm function. Overall, our results show no post-copulatory reproductive isolation between the lineages. How genetic differentiation in sympatry is maintained in the absence of a post-copulatory barrier between BL and HL remains to be investigated.

Asynchronous life cycles contribute to reproductive isolation between two Alpine butterflies.

Geographic isolation often leads to the emergence of distinct genetic lineages that are at least partially reproductively isolated. Zones of secondary contact between such lineages are natural experiments that allow investigation of how reproductive isolation evolves and co-existence is maintained. While temporal isolation through allochrony has been suggested to promote reproductive isolation in sympatry, its potential for isolation upon secondary contact is far less understood. Sampling two contact zones of a pair of mainly allopatric Alpine butterflies over several years and taking advantage of museum samples, we show that the contact zones have remained geographically stable over several decades. Furthermore, they seem to be maintained by the asynchronous life cycles of the two butterflies, with one reaching adulthood primarily in even and the other primarily in odd years. Genomic inferences document that allochrony is leaky and that gene flow from allopatric sites scales with the degree of geographic isolation. Overall, we show that allochrony has the potential to contribute to the maintenance of secondary contact zones of lineages that diverged in allopatry.

Sympatric and allopatric Alcolapia soda lake cichlid species show similar levels of assortative mating

Characterizing reproductive barriers such as mating preferences within rapid evolutionary radiations is crucial for understanding the early stages of speciation. Cichlid fishes are well-known for their adaptive radiations and capacity for rapid speciation and as such we investigate assortative mating among Alcolapia species; a recent (<10,000 years), small adaptive radiation, endemic to the extreme soda lakes, Magadi (one species) and Natron (three species), in East Africa. In seminatural aquarium conditions, we observed both courtship and mate choice (tested by microsatellite paternity analysis) to be significantly assortative among the three sympatric Natron species in a three-way choice experiment. This was also the case between allopatric species from Natron and Magadi, as found in a two-way choice experiment. However, the proportion of disassortative matings was substantial in both of these experiments, with hybrids comprising 29% of offspring in sympatric species and 11.4% in allopatric species comparisons. Previous work suggests that the Natron/Magadi split might not be much older than the radiation within Natron, so the similar rate of hybridization in the allopatric comparison is surprising and inconsistent with predictions of reinforcement theory, which predicts a faster rate of accumulation of premating isolation in sympatry. The relatively weak assortative mating in sympatry suggests that additional reproductive barriers, such as microhabitat preferences or spatial structuring may contribute to genetic isolation in nature.

Reproductive Character Displacement Drives Diversification of Male Courtship Songs in Drosophila.

AbstractMale secondary sexual traits are one of the most striking and diverse features of the animal kingdom. While these traits are often thought to evolve via sexual selection, many questions remain about their patterns of diversification and their role in speciation. To address these questions, I performed a comparative study of precopulatory male courtship songs of 119 Drosophila species across 10 distinct species groups. I related song divergence to genetic distances, geographic relationships, and sexual isolation between species. On the basis of pairwise Euclidean song distances, species groups typically retained their phylogenetic signal while species within groups diverged five times more in sympatry relative to allopatry, producing a pattern of reproductive character displacement. This occurred despite similar genetic distances in allopatry and sympatry, was exaggerated among younger species pairs, and was driven primarily by the parameter interpulse interval. While sexual isolation in sympatry was high even with low song divergence, these variables were correlated with each other and with increased divergence of female mating preferences in sympatry. The widespread pattern of character displacement implies that allopatric divergence due to processes like sexual selection are very slow relative to sympatric processes such as reinforcement and reproductive interference in driving song diversification across Drosophila.

Illuminating the incredible journey of pollen

Illuminating the incredible journey of pollen

Genomic Resources for Darters (Percidae: Etheostominae) Provide Insight into Postzygotic Barriers Implicated in Speciation.

Comparative genomic approaches are increasingly being used to study the evolution of reproductive barriers in nonmodel species. Although numerous studies have examined prezygotic isolation in darters (Percidae), investigations into postzygotic barriers have remained rare due to long generation times and a lack of genomic resources. Orangethroat and rainbow darters naturally hybridize and provide a remarkable example of male-driven speciation via character displacement. Backcross hybrids suffer from high mortality, which appears to promote behavioral isolation in sympatry. To investigate the genomic architecture of postzygotic isolation, we used Illumina and PacBio sequencing to generate a chromosome-level, annotated assembly of the orangethroat darter genome and high-density linkage maps for orangethroat and rainbow darters. We also analyzed genome-wide RADseq data from wild-caught adults of both species and laboratory-generated backcrosses to identify genomic regions associated with hybrid incompatibles. Several putative chromosomal translocations and inversions were observed between orangethroat and rainbow darters, suggesting structural rearrangements may underlie postzygotic isolation. We also found evidence of selection against recombinant haplotypes and transmission ratio distortion in backcross hybrid genomes, providing further insight into the genomic architecture of genetic incompatibilities. Notably, regions with high levels of genetic divergence between species were enriched for genes associated with developmental and meiotic processes, providing strong candidates for postzygotic isolating barriers. These findings mark significant contributions to our understanding of the genetic basis of reproductive isolation between species undergoing character displacement. Furthermore, the genomic resources presented here will be instrumental for studying speciation in darters, the most diverse vertebrate group in North America.

The evolution of male and female mating preferences in Drosophila speciation.

The relative importance of male and female mating preferences in causing sexual isolation between species remains a major unresolved question in speciation. Despite previous work showing that male courtship bias and/or female copulation bias for conspecifics occur in many taxa, the present study is one of the first large-scale works to study their relative divergence. To achieve this, we used data from the literature and present experiments across 66 Drosophila species pairs. Our results revealed that male and female mate preferences are both ubiquitous in Drosophila but evolved largely independently, suggesting different underlying evolutionary and genetic mechanisms. Moreover, their relative divergence strongly depends on the geographical relationship of species. Between allopatric species, male courtship and female copulation preferences diverged at very similar rates, evolving approximately linearly with time of divergence. In sharp contrast, between sympatric species pairs, female preferences diverged much more rapidly than male preferences and were the only drivers of enhanced sexual isolation in sympatry and Reproductive Character Displacement (RCD). Not only does this result suggest that females are primarily responsible for such processes as reinforcement, but it also implies that evolved female preferences may reduce selection for further divergence of male courtship preferences in sympatry.

Divergence in Potential Contact Pheromones and Genital Morphology Among Sympatric Song Types of the Bush Cricket Mecopoda elongata

A well-established route to speciation in animals is via the evolution of divergent male mating signals and female preferences within a species. However, an open question is how common it is for near complete isolation to be achieved through a single signal-receiver system or whether multiple aspects of the mate-recognition system diverge simultaneously. The five highly divergent song types of the bush cricket Mecopoda elongata, exemplify reproductive isolation in sympatry through long-distance mating signals. Female preference for their own song type has been established as a strong pre-mating reproductive barrier, but the potential existence of additional isolating mechanisms has not been investigated. We quantify divergence in cuticular lipid profiles and external genital structures between song types. These traits show significant divergence among species of Orthoptera and are known to be used in mate recognition following contact. We show that divergence among sympatric Mecopoda song types in both cuticular lipid profiles and two external genital structures is sufficiently extensive that either of them can be used to identify individual song type with 90% accuracy. Our findings suggest that multiple isolating mechanisms are likely to evolve simultaneously to facilitate a more robust reproductive isolation. This indicates a role for sexual selection in the divergence and potential future speciation of these populations and suggests that reproductive isolation may frequently evolve through simultaneous divergence across different aspects of mate recognition systems.

Hybridization and postzygotic isolation promote reinforcement of male mating preferences in a diverse group of fishes with traditional sex roles.

Behavioral isolation is thought to arise early in speciation due to differential sexual and/or natural selection favoring different preferences and traits in different lineages. Instead, behavioral isolation can arise due to reinforcement favoring traits and preferences that prevent maladaptive hybridization. In darters, female preference for male coloration has been hypothesized to drive speciation, because behavioral isolation evolves before F1 inviability. However, as with many long‐lived organisms, the fitness of second‐generation hybrids has not been assessed because raising animals to adulthood in the laboratory is challenging. Of late, reinforcement of male preferences has been implicated in darters because male preference for conspecific females is high in sympatry but absent in allopatry in multiple species pairs. The hypothesis that reinforcement accounts for behavioral isolation in sympatry assumes that hybridization and postzygotic isolation are present. Here, we used genomic and morphological data to demonstrate that hybridization is ongoing between orangethroat and rainbow darters and used hybrids collected from nature to measure postzygotic barriers across two hybrid generations. We observed sex ratio distortion in adult F1s and a dramatic reduction in backcross survival. Our findings indicate that selection to avoid hybridization promotes the evolution of male‐driven behavioral isolation via reinforcement in this system.

Rapid sexual and genomic isolation in sympatric Drosophila without reproductive character displacement.

The rapid evolution of sexual isolation in sympatry has long been associated with reinforcement (i.e., selection to avoid maladaptive hybridization). However, there are many species pairs in sympatry that have evolved rapid sexual isolation without known costs to hybridization. A major unresolved question is what evolutionary processes are involved in driving rapid speciation in such cases. Here, we focus on one such system; the Drosophila athabasca species complex, which is composed of three partially sympatric and interfertile semispecies: WN, EA, and EB. To study speciation in this species complex, we assayed sexual and genomic isolation within and between these semispecies in both sympatric and allopatric populations. First, we found no evidence of reproductive character displacement (RCD) in sympatric zones compared to distant allopatry. Instead, semispecies were virtually completely sexually isolated from each other across their entire ranges. Moreover, using spatial approaches and coalescent demographic simulations, we detected either zero or only weak heterospecific gene flow in sympatry. In contrast, within each semispecies we found only random mating and little population genetic structure, except between highly geographically distant populations. Finally, we determined that speciation in this system is at least an order of magnitude older than previously assumed, with WN diverging first, around 200K years ago, and EA and EB diverging 100K years ago. In total, these results suggest that these semispecies should be given full species status and we adopt new nomenclature: WN—D. athabasca, EA—D. mahican, and EB—D. lenape. While the lack of RCD in sympatry and interfertility do not support reinforcement, we discuss what additional evidence is needed to further decipher the mechanisms that caused rapid speciation in this species complex.

Genomic variation across two barn swallow hybrid zones reveals traits associated with divergence in sympatry and allopatry

Hybrid zones are geographic regions where isolating barriers between divergent populations are challenged by admixture. Identifying factors that facilitate or inhibit hybridization in sympatry can illuminate the processes that maintain those reproductive barriers. We analysed patterns of hybridization and phenotypic variation across two newly discovered hybrid zones between three subspecies of barn swallow (Hirundo rustica). These subspecies differ in ventral coloration and wing length, traits that are targets of sexual and natural selection, respectively, and are associated with genome-wide differentiation in allopatry. We tested the hypothesis that the degree of divergence in these traits is associated with the extent of hybridization in secondary contact. We applied measures of population structure based on >23,000 SNPs to confirm that named subspecies correspond to distinct genomic clusters, and assessed coincidence between geographic clines for ancestry and phenotype. Although gene flow was ongoing across both hybrid zones and pairwise FST between subspecies was extremely low, we found striking differences in the extent of hybridization. In the more phenotypically differentiated subspecies pair, clines for ancestry, wing length and ventral coloration were steep and coincident, suggestive of strong isolation and, potentially, selection associated with phenotype. In the less phenotypically differentiated pair, gene flow and phenotypic variation occurred over a wide geographic span, indicative of weaker isolation. Traits associated with genome-wide differentiation in allopatry may thus also contribute to isolation in sympatry. We discuss potentially important additional roles for evolutionary history and ecology in shaping variation in the extent hybridization between closely related pairs of subspecies.

Factors contributing to the accumulation of reproductive isolation: A mixed model approach.

The analysis of large datasets describing reproductive isolation between species has been extremely influential in the study of speciation. However, the statistical methods currently used for these data limit the ability to make direct inferences about the factors predicting the evolution of reproductive isolation. As a result, our understanding of iconic patterns and rules of speciation rely on indirect analyses that have clear statistical limitations. Phylogenetic mixed models are commonly used in ecology and evolution, but have not been applied to studies of reproductive isolation. Here I describe a flexible framework using phylogenetic mixed models to analyze data collected at different evolutionary scales, to test both categorical and continuous predictor variables, and to test the effect of multiple predictors on rates and patterns of reproductive isolation simultaneously. I demonstrate the utility of this framework by re‐analyzing four classic datasets, from both animals and plants, and evaluating several hypotheses that could not be tested in the original studies: In the Drosophila and Bufonidae datasets, I found support for more rapid accumulation of reproductive isolation in sympatric species pairs compared to allopatric species pairs. Using Silene and Nolana, I found no evidence supporting the hypothesis that floral differentiation elevates postzygotic reproductive isolation. The faster accumulation of postzygotic isolation in sympatry is likely the result of species coexistence determined by the level of postzygotic isolation between species. In addition, floral trait divergence does not appear to translate into pleiotropic effects on postzygotic reproductive isolation. Overall, these methods can allow researchers to test new hypotheses using a single statistical method, while remedying the statistical limitations of several previous methods.

The role of courtship song in female mate choice in South American Cactophilic Drosophila.

Courtship songs have undergone a spectacular diversification in the Drosophila buzzatii cluster. Accordingly, it has been suggested that sexual selection has played a significant role in promoting rapid diversification, reproductive isolation and speciation. However, there is no direct evidence (i.e., song playback experiments with wingless males) supporting this tenet. Moreover, several studies have showed that the courtship song in the genus Drosophila is not always used in female mate choice decisions, nor plays the same role when it is taken into account. In this vein, we use an approach that combines manipulative and playback experiments to explore the importance and the role of courtship song in female mate choice in four species of the D. buzzatii cluster and one species of the closely related D. martensis cluster for outgroup comparison. We also investigate the importance of courtship song in sexual isolation in sympatry between the only semi-cosmopolitan species, D. buzzatii, and the other species of the D. buzzatii cluster. Our study revealed that the courtship song is used by females of the D. buzzatii cluster as a criterion for male acceptance or influences the speed with which males are chosen. In contrast, we showed that this characteristic is not shared by D. venezolana, the representative species of the D. martensis cluster. We also found that the studied species of the D. buzzatii cluster differ in the role that conspecific and heterospecific songs have in female mate choice and in sexual isolation. Our findings support the hypothesis that divergence in female preferences for courtship songs has played a significant role in promoting rapid diversification and reproductive isolation in the D. buzzatii cluster. However, evidence from D. venezolana suggests that the use of the courtship song in female mate choice is not a conserved feature in the D. buzzatii complex.

The genetic architecture of local adaptation and reproductive isolation in sympatry within the Mimulus guttatus species complex.

The genetic architecture of local adaptation has been of central interest to evolutionary biologists since the modern synthesis. In addition to classic theory on the effect size of adaptive mutations by Fisher, Kimura and Orr, recent theory addresses the genetic architecture of local adaptation in the face of ongoing gene flow. This theory predicts that with substantial gene flow between populations local adaptation should proceed primarily through mutations of large effect or tightly linked clusters of smaller effect loci. In this study, we investigate the genetic architecture of divergence in flowering time, mating system-related traits, and leaf shape between Mimulus laciniatus and a sympatric population of its close relative M.guttatus. These three traits are probably involved in M.laciniatus' adaptation to a dry, exposed granite outcrop environment. Flowering time and mating system differences are also reproductive isolating barriers making them 'magic traits'. Phenotypic hybrids in this population provide evidence of recent gene flow. Using next-generation sequencing, we generate dense SNP markers across the genome and map quantitative trait loci (QTLs) involved in flowering time, flower size and leaf shape. We find that interspecific divergence in all three traits is due to few QTL of large effect including a highly pleiotropic QTL on chromosome 8. This QTL region contains the pleiotropic candidate gene TCP4 and is involved in ecologically important phenotypes in other Mimulus species. Our results are consistent with theory, indicating that local adaptation and reproductive isolation with gene flow should be due to few loci with large and pleiotropic effects.

Weaving a Tangled Web: Divergent and Reticulate Speciation in <I>Boechera fendleri</I> sensu lato (Brassicaceae: Boechereae)

Abstract Hybrid speciation is relatively common in plants compared to other well-studied groups. Polyploidy and apomixis are strongly associated with hybrid speciation, presumably due to the opportunities they provide for both reestablishing reproductive function in hybrids with incomplete chromosomal homology and creating rapid reproductive isolation in sympatry. Boechera, a species-rich genus closely related to Arabidopsis, is a particularly fertile ground for the study of hybrid speciation. Thirty-eight apomictic triploid hybrid species are currently recognized in Boechera. Recent research has shown that apomictic diploid hybrids, although very rare in angiosperms, are common in Boechera. Given this complexity, focused studies of individual species complexes are critical to understanding speciation and diagnosing biodiversity in Boechera. Here we analyze DNA sequences from seven nuclear loci and multilocus genotypes from 15 microsatellite markers in a group of closely related taxa formerly included in ...

ON THE COYNE AND ORR-IGIN OF SPECIES: EFFECTS OF INTRINSIC POSTZYGOTIC ISOLATION, ECOLOGICAL DIFFERENTIATION, X CHROMOSOME SIZE, AND SYMPATRY ONDROSOPHILASPECIATION

Coyne and Orr found that mating discrimination (premating isolation) evolves much faster between sympatric than allopatric Drosophila species pairs. Their meta-analyses established that this pattern, expected under reinforcement, is common and that Haldane's rule is ubiquitous in Drosophila species divergence. We examine three possible contributors to the reinforcement pattern: intrinsic postzygotic isolation, dichotomized as to whether hybrid males show complete inviability/sterility; host-plant divergence, as a surrogate for extrinsic postzygotic isolation; and X chromosome size, whether roughly 20% or 40% of the genome is X-linked. We focus on "young" species pairs with overlapping ranges, contrasted with allopatric pairs. Using alternative criteria for "sympatry" and tests that compare either level of prezygotic isolation in sympatry or frequency of sympatry, we find no statistically significant effects associated with X chromosome size or our coarse quantifications of intrinsic postzygotic isolation or ecological differentiation. Although sympatric speciation seems very rare in animals, the pervasiveness of the reinforcement pattern and the commonness of range overlap for close relatives indicate that speciation in Drosophila is often not purely allopatric. It remains to determine whether increased premating isolation with sympatry results from secondary contact versus parapatric speciation and what drives this pattern.

Ecological adaptation and reproductive isolation in sympatry: genetic and phenotypic evidence for native host races of Rhagoletis pomonella

Ecological speciation with gene flow may be an important mode of diversification for phytophagous insects. The recent shift of Rhagoletis pomonella from its native host downy hawthorn (Crataegus mollis) to introduced apple (Malus domestica) in the northeastern United States is a classic example of sympatric host race formation. Here, we test whether R. pomonella has similarly formed host races on four native Crataegus species in the southern United States: western mayhaw (C. opaca), blueberry hawthorn (C. brachyacantha), southern red hawthorn (C. mollis var. texana) and green hawthorn (C. viridis). These four southern hosts differ from each other in their fruiting phenology and in the volatile compounds emitted from the surface of their fruits. These two traits form the basis of ecological reproductive isolation between downy hawthorn and apple flies in the north. We report evidence from microsatellite population surveys and eclosion studies supporting the existence of genetically differentiated and partially reproductively isolated host races of southern hawthorn flies. The results provide an example of host shifting and ecological divergence involving native plants and imply that speciation with gene flow may be commonly initiated in Rhagoletis when ecological opportunity presents itself.