Extensive loss of Wnt genes in Tardigrada

Evolution of reproductive isolation is an important process, generating biodiversity and driving speciation. To better understand this process, it is necessary to investigate factors underlying reproductive isolation through various approaches but also in various taxa. Previous studies, mainly focusing on diploid animals, supported the prevalent view that reproductive barriers evolve gradually as a by-product of genetic changes accumulated by natural selection by showing a positive relationship between the degree of reproductive isolation and genetic distance. Haplodiploid animals are expected to generate additional insight into speciation, but few studies investigated the prevalent view in haplodiploid animals. In this study, we investigate whether the relationship also holds in a haplodiploid spider mite, Amphitetranychus viennensis (Zacher). We sampled seven populations of the mite in the Palaearctic region, measured their genetic distance (mtDNA) and carried out cross experiments with all combinations. We analyzed how lack of fertilization rate (as measure of prezygotic isolation) as well as hybrid inviability and hybrid sterility (as measures of postzygotic isolation) varies with genetic distance. We found that the degree of reproductive isolation varies among cross combinations, and that all three measures of reproductive isolation have a positive relationship with genetic distance. Based on the mtDNA marker, lack of fertilization rate, hybrid female inviability and hybrid female sterility were estimated to be nearly complete (99.0–99.9% barrier) at genetic distances of 0.475–0.657, 0.150–0.209 and 0.145–0.210, respectively. Besides, we found asymmetries in reproductive isolation. The prevalent view on the evolution of reproductive barriers is supported in the haplodiploid spider mite we studied here. According to the estimated minimum genetic distance for total reproductive isolation in parent population crosses in this study and previous work, a genetic distance of 0.15–0.21 in mtDNA (COI) appears required for speciation in spider mites. Variations and asymmetries in the degree of reproductive isolation highlight the importance of reinforcement of prezygotic reproductive isolation through incompatibility and the importance of cytonuclear interactions for reproductive isolation in haplodiploid spider mites.     

Reproductive isolating barriers between colour‐differentiated populations of an African annual killifish,Nothobranchius korthausae (Cyprinodontiformes)

Allopatric populations separated by vicariance events are expected to evolve reproductive isolating mechanisms as a result of disparate selection pressures and genetic drift. The appearance of reproductive isolating mechanisms may vary across taxa with differences in the opportunity for mate choice, and may be asymmetrical. In addition, premating barriers may be affected by individual mating experience. We used choice and no‐choice experiments to investigate reproductive isolation between two allopatric (island and mainland) and colour‐differentiated populations of an African annual fish, Nothobranchius korthausae. Assortative mating under experimental conditions was limited and asymmetrical. Preference for sympatric males was only expressed in nonvirgin females from one population. Virgin fish from both populations mated indiscriminately. No difference in the number of eggs laid, fertilization rate and hatching success was detected in no‐choice experiments. All mating combinations produced viable offspring and no postmating barriers were detected in terms of the performance and fertility of F1 hybrids. Overall, we found little evidence for significant reproductive isolation, which is in contrast with the related killifish taxa in which assortative mating can be strong, even among allopatric populations with no colour differentiation. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 62–72.     

Premating, not postmating, barriers drive genetic dynamics in experimental hybrid populations of the endangered Sonoran topminnow

The timing and pattern of reproductive barrier formation in allopatric populations has received much less attention than the accumulation of reproductive barriers in sympatry. The theory of allopatric speciation suggests that reproductive barriers evolve simply as by-products of overall genetic divergence. However, observations of enhanced premating barriers in allopatric populations suggest that sexual selection driven by intraspecific competition for mates may enhance species-specific signals and accelerate the speciation process. In a previous series of laboratory trials, we examined the strength of premating and postmating barriers in an allopatric species pair of the endangered Sonoran topminnow, Poeciliopsis occidentalis and P. sonoriensis. Behavioral observations provided evidence of asymmetrical assortative mating, while reduced brood sizes and male-biased F(1) sex ratios suggest postmating incompatibilities. Here we examine the combined effects of premating and postmating barriers on the genetic makeup of mixed populations, using cytonuclear genotype frequencies of first- and second-generation offspring. Observed genotype frequencies strongly reflect the directional assortative mating observed in behavioral trials, illustrating how isolating barriers that act earlier in the reproductive cycle will have a greater effect on total reproductive isolation and may be more important to speciation than subsequent postmating reproductive barriers.     

Patterns of reproductive isolation in three angiosperm genera

Analyses among animal species have found that reproductive isolation increases monotonically with genetic distance, evolves more quickly for prezygotic than postzygotic traits, and is stronger among sympatric than allopatric species pairs. The latter pattern is consistent with expectations under the reinforcement hypothesis. To determine whether similar trends are found among plant species, patterns of reproductive isolation (postpollination prezygotic, postzygotic, and "total" isolation) in three plant genera (Glycine, Silene, Streptanthus) were examined using data from previously published artificial hybridization experiments. In Silene, all measures of reproductive isolation were positively correlated with genetic distance. In contrast, in Glycine and Streptanthus, correlations between reproductive isolation and genetic distance were weak or nonsignificant, possibly due to the influence of biologically unusual taxa, variable evolutionary forces acting in different lineages, or insufficient time to accumulate reproductive isolation. There was no evidence that postpollination prezygotic reproductive isolation evolved faster than postzygotic isolation in Glycine or Silene. We also detected no evidence for faster accumulation of postmating prezygotic isolation between sympatric than allopatric species pairs; thus we found no evidence for the operation of speciation via reinforcement. In Silene, which included six polyploid species, results suggest that changes in ploidy disrupt a simple monotonic relationship between isolation and genetic distance.     

Review. The strength and genetic basis of reproductive isolating barriers in flowering plants

Speciation is characterized by the evolution of reproductive isolation between two groups of organisms. Understanding the process of speciation requires the quantification of barriers to reproductive isolation, dissection of the genetic mechanisms that contribute to those barriers and determination of the forces driving the evolution of those barriers. Through a comprehensive analysis involving 19 pairs of plant taxa, we assessed the strength and patterns of asymmetry of multiple prezygotic and postzygotic reproductive isolating barriers. We then reviewed contemporary knowledge of the genetic architecture of reproductive isolation and the relative role of chromosomal and genic factors in intrinsic postzygotic isolation. On average, we found that prezygotic isolation is approximately twice as strong as postzygotic isolation, and that postmating barriers are approximately three times more asymmetrical in their action than premating barriers. Barriers involve a variable number of loci, and chromosomal rearrangements may have a limited direct role in reproductive isolation in plants. Future research should aim to understand the relationship between particular genetic loci and the magnitude of their effect on reproductive isolation in nature, the geographical scale at which plant speciation occurs, and the role of different evolutionary forces in the speciation process.     

Possible glimpses into early speciation: the effect of ovarian fluid on sperm velocity accords with post‐copulatory isolation between two guppy populations

Identifying mechanisms of reproductive isolation is key to understanding speciation. Among the putative mechanisms underlying reproductive isolation, sperm–female interactions (post‐mating–prezygotic barriers) are arguably the hardest to identify, not least because these are likely to operate at the cellular or molecular level. Yet sperm–female interactions offer great potential to prevent the transfer of genetic information between different populations at the initial stages of speciation. Here, we provide a preliminary test for the presence of a putative post‐mating–prezygotic barrier operating between three populations of Trinidadian guppies (Poecilia reticulata), an internally fertilizing fish that inhabits streams with different levels of connectivity across Trinidad. We experimentally evaluate the effect of female ovarian fluid on sperm velocity (a predictor of competitive fertilization success) according to whether males and females were from the same (native) or different (foreign) populations. Our results reveal the potential for ovarian fluid to act as a post‐mating–prezygotic barrier between two populations from different drainages, but also that the strength of this barrier is different among populations. This result may explain the previous finding that, in some populations, sperm from native males have precedence over foreign sperm, which could eventually lead to reproductive isolation between these populations.     

Rapid evolution of prezygotic barriers in non‐territorial damselflies

A central question in evolutionary biology concerns the accumulation of reproductive barriers during speciation. However, separating the reproductive barriers that have led to speciation from those that have secondarily accumulated (i.e. after initial divergence) is a widely recognized problem. Ideal candidate species for overcoming this problem are young species, where time for additional barriers to accrue has been limited. In the present study, we add to previous studies investigating the strength of reproductive barriers between the parapatric damselflies Ischnura elegans and Ischnura graellsii by quantifying seven prezygotic barriers between the allopatric pairs of I. elegans and Ischnura genei, as well as I. graellsii and I. genei. Specifically, we measured four premating (temporal, sexual, mechanical _I, and mechanical _II) and three postmating (oviposition success, fecundity, and fertility) barriers using experimental approaches and, for first time, we investigated the mechanisms causing mechanical isolation, which is the strongest reproductive barrier in ischnurans. The findings of the present study support the notion that premating barriers are generally strong and contribute significantly to total reproductive isolation in young lineages (65–98%), although they never solely lead to complete isolation. Asymmetry was generally stronger in premating than in postmating barriers, and was driven mostly through asymmetry in mechanical isolation, which is caused by morphological divergence of secondary sexual appendages. We found that barriers act multiplicatively in all species combinations tested, with the exception of sexual isolation, which was not detected. Our results are consistent with a recent allopatric speciation scenario driven by differences in male anal appendages, either impeding copulation or affecting female preferences. Taken together, the results from this and previous studies in diverse odonate genera suggest that premating barriers have evolved rapidly in ischnuran damselflies and, although reproductive isolation in ischnurans is more commonly the result of several barriers acting together, morphological divergence of secondary sexual appendages appears to be a common factor facilitating premating isolation in this group. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 485–496.     

Patterns of reproductive isolation in Mediterranean deceptive orchids

The evolution of reproductive isolation is of central interest in evolutionary biology. In plants, this is typically achieved by a combination of pre- and postpollination mechanisms that prevent, or limit, the amount of interspecific gene flow. Here, we investigated and compared two ecologically defined groups of Mediterranean orchids that differ in pollination biology and pollinator specificity: sexually deceptive orchids versus food-deceptive orchids. We used experimental crosses to assess the strength of postmating prezygotic, and postzygotic reproductive isolation, and a phylogenetic framework to determine their relative rates of evolution. We found quantitative and qualitative differences between the two groups. Food-deceptive orchids have weak premating isolation but strong postmating isolation, whereas the converse situation characterizes sexually deceptive orchids. Only postzygotic reproductive isolation among food-deceptive orchids was found to evolve in a clock-like manner. Comparison of evolutionary rates, within a common interval of genetic distance, showed that the contribution of postmating barriers was more relevant in the food-deceptive species than in the sexually deceptive species. Asymmetry in prezygotic isolation was found among food-deceptive species. Our results indicate that postmating barriers are most important for reproductive isolation in food-deceptive orchids, whereas premating barriers are most important in sexually deceptive orchids. The different rate of evolution of reproductive isolation and the relative strength of pre- and postmating barriers may have implication for speciation processes in the two orchid groups.     

PATTERNS OF SPECIATION IN DROSOPHILA

To investigate the time course of speciation, we gathered literature data on 119 pairs of closely related Drosophila species with known genetic distances, mating discrimination, strength of hybrid sterility and inviability, and geographic ranges. Because genetic distance is correlated with divergence time, these data provide a cross-section of taxa at different stages of speciation. Mating discrimination and the sterility or inviability of hybrids increase gradually with time. Hybrid sterility and inviability evolve at similar rates. Among allopatric species, mating discrimination and postzygotic isolation evolve at comparable rates, but among sympatric species strong mating discrimination appears well before severe sterility or inviability. This suggests that prezygotic reproductive isolation may be reinforced when allopatric taxa become sympatric. Analysis of the evolution of postzygotic isolation shows that recently diverged taxa usually produce sterile or inviable male but not female hybrids. Moreover, there is a large temporal gap between the evolution of male-limited and female hybrid sterility or inviability. This gap, which is predicted by recent theories about the genetics of speciation, explains the overwhelming preponderance of hybridizations yielding male-limited hybrid sterility or inviability (Haldane's rule).     

Hybrid sterility and inviability in the parasitic fungal species complex Microbotryum

Microbotryum violaceum, the anther‐smut fungus, forms a complex of sibling species which specialize on different plants. Previous studies have shown the presence of partial ecological isolation and F1 inviability, but did not detect assortative mating apart from a high selfing rate. We investigated other post‐mating barriers and show that F1 hybrid sterility, the inability of gametes to mate, increased gradually with the increasing genetic distance between the parents. F2 hybrids showed a reduced ability to infect the plants that was also correlated with the genetic distance. The host on which the F2 hybrids were passaged caused a selection for alleles derived from the pathogen species originally isolated from that host, but this effect was not detectable for the most closely related species. The post‐mating barriers thus remain weak among the closest species pairs, suggesting that premating barriers are sufficient to initiate divergence in this system.     

Phenotypic divergence but not genetic distance predicts assortative mating among species of a cichlid fish radiation

The hypothesis of ecological divergence giving rise to premating isolation in the face of gene flow is controversial. However, this may be an important mechanism to explain the rapid multiplication of species during adaptive radiation following the colonization of a new environment when geographical barriers to gene flow are largely absent but underutilized niche space is abundant. Using cichlid fish, we tested the prediction of ecological speciation that the strength of premating isolation among species is predicted by phenotypic rather than genetic distance. We conducted mate choice experiments between three closely related, sympatric species of a recent radiation in Lake Mweru (Zambia/DRC) that differ in habitat use and phenotype, and a distantly related population from Lake Bangweulu that resembles one of the species in Lake Mweru. We found significant assortative mating among all closely related, sympatric species that differed phenotypically, but none between the distantly related allopatric populations of more similar phenotype. Phenotypic distance between species was a good predictor of the strength of premating isolation, suggesting that assortative mating can evolve rapidly in association with ecological divergence during adaptive radiation. Our data also reveals that distantly related allopatric populations that have not diverged phenotypically, may hybridize when coming into secondary contact, e.g. upon river capture because of diversion of drainage systems.     

Postmating barriers to hybridization between an island’s native eucalypts and an introduced congener

We evaluate postmating barriers to hybridization between an exotic eucalypt and a group of native congeners on the island of Tasmania. We aimed to better understand the basis of reproductive isolation between the species, glean insights into the evolution of isolating mechanisms, and inform genetic risk management. Compatibility between the exotic plantation species Eucalyptus nitens (pollen parent) and 18 native Tasmanian taxa was assayed using experimental crossing for 17 taxa (13,458 flowers pollinated to produce 1058 female × male cross combinations), and previous data for one species. Compatibility was assessed in terms of F₁ hybrid production, as well as F₁ hybrid survival and growth after 5 years. This data was combined with measurements of style length, and genetic distance from E. nitens to each maternal species, in order to determine the importance of a sequence of prezygotic and postzygotic barriers. We found that the early-acting barrier of style length (prezygotic) had the strongest isolating effect, while later-acting (postzygotic) barriers, affecting early-age growth and survival, contributed little to reproductive isolation. Style length alone explained 46 % of the variation in hybridization rate. Conversely, there was no significant relationship between genetic distance and prezygotic or postzygotic compatibility in these closely related species. This pattern is consistent with selection driving the rapid evolution of prezygotic barriers, while drift-like-processes lead to the more gradual evolution of intrinsic barriers. Although other premating and postmating barriers clearly contribute, our results highlight the important role of early-acting postmating barriers in preventing gene flow from exotic E. nitens plantations.     

Strong premating reproductive isolation drives incipient speciation in Mimulus aurantiacus

Determining which forms of reproductive isolation have the biggest impact on the process of divergence is a major goal of speciation research. These barriers are often divided into those that affect the potential for hybridization (premating isolation), and those that occur after mating (postmating isolation), and much debate has surrounded the relative importance of these categories. Within the species Mimulus aurantiacus, red‐ and yellow‐flowered ecotypes occur in the southwest corner of California, and a hybrid zone occurs where their ranges overlap. We show that premating barriers are exclusively responsible for isolation in this system, with both ecogeographic and pollinator isolation contributing significantly to total isolation. Postmating forms of reproductive isolation have little or no impact on gene flow, indicating that hybrids likely contribute to introgression at neutral loci. Analysis of molecular variation across thousands of restriction‐site associated DNA sequencing (RAD‐seq) markers reveals that the genomes of these taxa are largely undifferentiated. However, structure analysis shows that these taxa are distinguishable genetically, likely due to the impact of loci underlying differentiated adaptive phenotypes. These data exhibit the power of divergent natural selection to maintain highly differentiated phenotypes in the face of gene flow during the early stages of speciation.     

Existence of a pattern of reproductive character displacement in Homobasidiomycota but not in Ascomycota

Generally, stronger reproductive isolation is expected between sympatric than between allopatric sibling species. Such reproductive character displacement should predominantly affect premating reproductive isolation and can be due to several mechanisms, including population extinction, fusion of insufficiently isolated incipient species and reinforcement of reproductive isolation in response to low hybrid fitness. Experimental data on several taxa have confirmed these theoretical expectations on reproductive character displacement, but they are restricted to animals and a few plants. Using results reported in the literature on crossing experiments in fungi, we compared the degree and the nature of reproductive isolation between allopatric and sympatric species pairs. In accordance with theoretical expectations, we found a pattern of enhanced premating isolation among sympatric sibling species in Homobasidiomycota. By contrast, we did not find evidence for reproductive character displacement in Ascomycota at similar genetic distances. Both allopatric and sympatric species of Ascomycota had similarly low levels of reproductive isolation, being mostly post-zygotic. This suggests that some phylogeny-dependent life-history trait may strongly influence the evolution of reproductive isolation between closely related species. A significant correlation was found between degree of reproductive isolation and genetic divergence among allopatric species of Homobasidiomycota, but not among sympatric ones or among Ascomycota species.     

Evolution of reproductive isolation in plants

Reproductive isolation is essential for the process of speciation and much has been learned in recent years about the ecology and underlying genetics of reproductive barriers. But plant species are typically isolated not by a single factor, but by a large number of different pre- and postzygotic barriers, and their potentially complex interactions. This phenomenon has often been ignored to date. Recent studies of the relative importance of different isolating barriers between plant species pairs concluded that prezygotic isolation is much stronger than postzygotic isolation. But studies of the patterns of reproductive isolation in plants did not find that prezygotic isolation evolves faster than postzygotic isolation, in contrast to most animals. This may be due to the multiple premating barriers that isolate most species pairs, some of which may be controlled by few genes of major effect and evolve rapidly, whereas others have a complex genetic architecture and evolve more slowly. Intrinsic postzygotic isolation in plants is correlated with genetic divergence, but some instrinsic postzygotic barriers evolve rapidly and are polymorphic within species. Extrinsic postzygotic barriers are rarely included in estimates of different components of reproductive isolation. Much remains to be learned about ecological and molecular interactions among isolating barriers. The role of reinforcement and reproductive character displacement in the evolution of premating barriers is an open topic that deserves further study. At the molecular level, chromosomal and genic isolation factors may be associated and act in concert to mediate reproductive isolation, but their interactions are only starting to be explored.     

Postmating reproductive barriers contribute to the incipient sexual isolation of the United States and Caribbean Drosophila melanogaster

The nascent stages of speciation start with the emergence of sexual isolation. Understanding the influence of reproductive barriers in this evolutionary process is an ongoing effort. We present a study of Drosophila melanogaster admixed populations from the southeast United States and the Caribbean islands known to be a secondary contact zone of European‐ and African‐derived populations undergoing incipient sexual isolation. The existence of premating reproductive barriers has been previously established, but these types of barriers are not the only source shaping sexual isolation. To assess the influence of postmating barriers, we investigated putative postmating barriers of female remating and egg‐laying behavior, as well as hatchability of eggs laid and female longevity after mating. In the central region of our putative hybrid zone of American and Caribbean populations, we observed lower hatchability of eggs laid accompanied by increased resistance to harm after mating to less‐related males. These results illustrate that postmating reproductive barriers act alongside premating barriers and genetic admixture such as hybrid incompatibilities and influence early phases of sexual isolation.     

Mating behaviour in the endangered Sonoran topminnow: speciation in action

Two species of the endangered Sonoran topminnow, Poeciliopsis occidentalis and P. sonoriensis, occur in two isolated drainage systems in southeast Arizona, U.S.A., and are allopatric throughout their range. Although these two taxa are morphologically very similar, and have been previously described as the same species or subspecies, several molecular studies have since indicated that they differ more than their morphology suggests. To determine whether the behaviours of the two species function as premating barriers to reproduction, we investigated their mating preferences and behavioural patterns in a laboratory setting. Results from no-choice mating observations showed that the mating behaviours of the two species differ. Observations conducted during multiple-choice mating trials provided evidence of assortative mating, suggesting an early stage of premating reproductive isolation.     

Reproductive isolation among allopatric Drosophila montana populations

An outstanding goal in speciation research is to trace the mode and tempo of the evolution of barriers to gene flow. Such research benefits from studying incipient speciation, in which speciation between populations has not yet occurred, but where multiple potential mechanisms of reproductive isolation (RI: i.e., premating, postmating‐prezygotic (PMPZ), and postzygotic barriers) may act. We used such a system to investigate these barriers among allopatric populations of Drosophila montana. In all heteropopulation crosses we found premating (sexual) isolation, which was either symmetric or asymmetric depending on the population pair compared. Postmating isolation was particularly strong in crosses involving males from one of the study populations, and while sperm were successfully transferred, stored, and motile, we experimentally demonstrated that the majority of eggs produced were unfertilized. Thus, we identified the nature of a PMPZ incompatibility. There was no evidence of intrinsic postzygotic effects. Measures of absolute and relative strengths of pre‐ and postmating barriers showed that populations differed in the mode and magnitude of RI barriers. Our results indicate that incipient RI among populations can be driven by different contributions of both premating and PMPZ barriers occurring between different population pairs and without the evolution of postzygotic barriers.     

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

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.     

Habitat preference and flowering‐time variation contribute to reproductive isolation between diploid and autotetraploid Anacamptis pyramidalis

Tetraploid lineages are typically reproductively isolated from their diploid ancestors by post‐zygotic isolation via triploid sterility. Nevertheless, polyploids often also exhibit ecological divergence that could contribute to reproductive isolation from diploid ancestors. In this study, we disentangled the contribution of different forms of reproductive isolation between sympatric diploid and autotetraploid individuals of the food‐deceptive orchid Anacamptis pyramidalis by quantifying the strength of seven reproductive barriers: three prepollination, one post‐pollination prezygotic and three post‐zygotic. The overall reproductive isolation between the two cytotypes was found very high, with a preponderant contribution of two prepollination barriers, that is phenological and microhabitat differences. Although the contribution of post‐zygotic isolation (triploid sterility) is confirmed in our study, these results highlight that prepollination isolation, not necessarily involving pollinator preference, can represent a strong component of reproductive isolation between different cytotypes. Thus, in the context of polyploidy as quantum speciation, that generates reproductive isolation via triploid sterility, ecological divergence can strengthen the reproductive isolation between cytotypes, reducing the waste of gametes in low fitness interploidy crosses and thus favouring the initial establishment of the polyploid lineage. Under this light, speciation by polyploidy involves ecological processes and should not be strictly considered as a nonecological form of speciation.