Hybrid zones and the speciation continuum in Heliconius butterflies

Tropical butterflies in the genus Heliconius have long been models in the study of the stages of speciation. Heliconius are unpalatable to predators, and many species are notable for multiple geographic populations with striking warning colour pattern differences associated with Müllerian mimicry. A speciation continuum is evident in Heliconius hybrid zones. Examples range from hybrid zones across which (a) there is little genetic differentiation other than at mimicry loci, but where hybrids are common, (b) to ‘bimodal‘ hybrid zones with strong genetic divergence and few hybrids, (c) through to ‘good’ sympatric species, with hybridization extremely rare or absent. Now, in this issue of Molecular Ecology, Arias et al. ( 2012 ) have found an intermediate case in Colombian Heliconius cydno showing evidence for assortative mating and molecular differences, but where hybrids are abundant.     

Characterizing patterns of introgressive hybridization between two species of Tyrannus following concurrent range expansion

Hybridization between two species typically occurs when allopatric or ecologically dissimilar species expand into areas of secondary contact or habitat transitions. However, as species' ranges shift rapidly in response to environmental change, the potential for novel types of ephemeral hybrid zones exists. Here, we document and describe the occurrence, prevalence and symmetry of a previously undocumented hybrid zone involving two sympatric, ecologically similar sister species that have been expanding their ranges eastward in the central USA: Scissor‐tailed Flycatchers Tyrannus forficatus and Western Kingbirds Tyrannus verticalis. We identified cases of hybridization and introgression using analyses of eight microsatellite DNA loci and a single mitochondrial gene. We also evaluated short‐term reproductive consequences of hybridization for both species by surveying for both species and potential hybrids at the periphery of their ranges in northeastern Arkansas and western Tennessee, USA. Genetic data revealed bi‐directional backcrossing at the periphery of the species’ ranges, including a cryptic hybrid. We also analysed DNA of putative ‘pure’ individuals from other parts of their ranges and detected two cryptic admixed individuals, suggesting backcrossed individuals from the periphery may be dispersing to breed or that hybridization events have occurred in the core. Finally, our results suggest that there are no short‐term reproductive consequences of hybridization for the two species. In total, hybrid zones that occur at the edges of expanding, sympatric ranges may be ephemeral; we suggest they play an important role in introgression and may have long‐standing impacts for sympatric sister species. Exploring the extent of hybrid zones such as this for other range‐expanding taxa will elucidate whether this type of hybrid zone is unique or a common occurrence.     

Hybridization dynamics between sympatric species of trout: loss of reproductive isolation

Although reinforcement should enhance reproductive barriers in sympatric species, sympatric trout species do hybridize. Using mitochondrial and nuclear species markers, we investigated hybridization directionality, hybrid mating biases, and selection against hybrids in 13 sympatric cut-throat and rainbow trout populations on Vancouver Island, Canada. Approximately 50% of the genotyped fish were hybrid (F1 or higher-order) and populations ranged from very recent (all F1 hybrids) to extremely advanced higher-order hybridization. Overall, interbreeding was reciprocal, although some populations showed directional hybridization. Pronounced cytonuclear disequilibrium in post-F1 hybrids indicated a remarkable mating bias not previously reported, which is most likely because of behavioural reproductive preferences. Selection against hybrids was observed in only two populations, indicative of extrinsic selection. Two populations were 'hybrid swarms', with a complete loss of reproductive isolation. The complex hybridization dynamics in this system represent a valuable natural experiment of the genetic and evolutionary implications of recent and on-going interspecific hybridization.     

Ecology and genetics of hybrid zones in the southern African Pycnonotus bulbul species complex

Lloyd, P., Craig, A.J.F.K., Hulley, P.E., Essop, M.F., Bloomer, P. & Crowe, T.M. 1997. Ecology and genetics of hybrid zones in the southern African Pycnonotus bulbul species complex. Ostrich 68 (2–4): 90–96.

The closely related Blackeyed Bulbul Pycnonotus barbatus, Cape Bulbul P. capensis and Redeyed Bulbul P. nigricans have parapatric to locally sympatric distributions within southern Africa. Extensive hybridization along narrow transition zones between each of the three species pairs is described in a region of the Eastern Cape province, South Africa. The transition zones coincide with ecotones between different vegetation types, which in turn follow escarpments or mountain ranges. The lack of population density depressions within the hybrid zones, together with the variability of the hybrids, suggests the hybrids are viable. Sharp step clines in various phenotypic characters are described across the P. barbatus/P. nigricans hybrid zone. A mtDNA analysis found evidence of possible introgression between P. barbatus and P. capensis. All eight P. barbatus x P. nigricans hybrids analysed possessed P. barbatus mtDNA, suggesting the existence of either positive assortative mating or strong directional selection, but our data are unable to distinguish which. Our results do not support the dynamic-equilibrium model, but are compatible with the bounded-hybrid-superiority model. We conclude that the maintenance of the parapatric distributions of the different taxa is due mainly to differences in environmentally-associated fitness between parental phenotypes or among parental and hybrid phenotypes along an ecotone, with the narrowness of the hybrid zones maintained by the steepness of the environmental gradients crossing them.     

Sympatric speciation in a genus of marine reef fishes

Sympatric speciation has been contentious since its inception, yet is increasingly recognized as important based on accumulating theoretical and empirical support. Here, we present a compelling case of sympatric speciation in a taxon of marine reef fishes using a comparative and mechanistic approach. Hexagrammos otakii and H. agrammus occur in sympatry throughout their ranges. Molecular sequence data from six loci, with complete sampling of the genus, support monophyly of these sister species. Although hybridization occurrs frequently with an allopatric congener in an area of slight distributional overlap, we found no F₁ hybrids between the focal sympatric taxa throughout their coextensive ranges. We present genetic evidence for complete reproductive isolation based on SNP analysis of 382 individuals indicating fixed polymorphisms, with no shared haplotypes or genotypes, between sympatric species. To address questions of speciation, we take a mechanistic approach and directly compare aspects of reproductive isolation between allopatric and sympatric taxa both in nature and in the laboratory. We conclude that the buildup of reproductive isolation is strikingly different in sympatric vs. allopatric taxa, consistent with theoretical predictions. Lab reared hybrids from allopatric species crosses exhibit severe fitness effects in the F₁ or backcross generation. No intrinsic fitness effects are observed in F₁ hybrids from sympatric species pairs, however these treatments exhibited reduced fertilization success and complete pre‐mating isolation is implied in nature because F₁ hybrid adults do not occur. Our study addresses limitations of previous studies and supports new criteria for inferring sympatric speciation.     

Biotope principles of sympatry and interspecies hybridization in mammals (by the example of the genus <Emphasis Type="Italic">Spermophilus</Emphasis>)

Two hybridization zones were taken as an example (the russet ground squirrel (Spermophilus major) and the speckled ground squirrel (S. suslicus), the russet ground squirrel and the yellow ground squirrel S. fulvus) to show that biotope characteristics determine segregation of sympatric species in contact colonies. The heterogeneity of biotopes with regard to the requirements of sympatric species promotes their long-term and steady dispersal and, in rare cases, sporadic hybridization. A biotope with a homogenous environment enables wide interspecies hybridization and a rapid increase in the ratio of hybrids in the colony.     

A test of hybrid growth disadvantage in wild, free-ranging species pairs of threespine stickleback (Gasterosteus aculeatus) and its implications for ecological speciation

Ecological speciation is the evolution of reproductive isolation as a direct or indirect consequence of divergent natural selection. Reduced performance of hybrids in nature is thought to be an important process by which natural selection can favor the evolution of assortative mating and drive speciation. Benthic and limnetic sympatric species of threespine stickleback (Gasterosteus aculeatus) are adapted to alternative trophic niches (bottom browsing vs. open water planktivory, respectively) and reduced feeding performance of hybrids is thought to have contributed to the evolution of reproductive isolation. We tested this “hybrid‐disadvantage hypothesis” by inferring growth rates from otoliths sampled from wild, free‐ranging benthic, limnetic, and hybrid sticklebacks in two lakes. There were significant differences in growth rate between lakes, life‐history stages, and among years (maximum P = 0.02), as well as interactions between most factors, but not between hybrid and parental species sticklebacks in most comparisons. Our results provide little evidence of a growth disadvantage in hybrid sticklebacks when free‐ranging in nature. Although trophic ecology per se may contribute less to ecological speciation than envisioned, it may act in concert with other aspects of stickleback biology, such as interactions with parasites, predators, competitors, and/or sexual selection, to present strong multifarious selection against hybrids.     

Genetic and morphological evidence of a geographically widespread hybrid zone between two crocodile species,Crocodylus acutus and Crocodylus moreletii

Hybrid zones represent natural laboratories to study gene flow, divergence and the nature of species boundaries between closely related taxa. We evaluated the level and extent of hybridization between Crocodylus moreletii and Crocodylus acutus using genetic and morphological data on 300 crocodiles from 65 localities. To our knowledge, this is the first genetic study that includes the entire historic range and sympatric zone of the two species. Contrary to expectations, Bayesian admixture proportions and maximum‐likelihood estimates of hybrid indexes revealed that most sampled crocodiles were admixed and that the hybrid zone is geographically extensive, extending well beyond their historical region of sympatry. We identified a few geographically isolated, nonadmixed populations of both parental species. Hybrids do not appear to be F₁s or recent backcrosses, but rather are more likely later‐generation hybrids, suggesting that hybridization has been going on for several to many generations and is mostly the result of natural processes. Crocodylus moreletii is not the sister species of C. acutus, suggesting that the hybrid zone formed from secondary contact rather than primary divergence. Nonadmixed individuals from the two species were distinguishable based on morphological characters, whereas hybrids had a complex mosaic of morphological characters that hinders identification in the wild. Very few nonadmixed C. acutus and C. moreletii populations exist in the wild. Consequently, the last nonadmixed C. moreletii populations have become critically endangered. Indeed, not only the parental species but also the naturally occurring hybrids should be considered for their potential conservation value.     

Low levels of hybridization across two contact zones among three species of woodpeckers (Sphyrapicus sapsuckers)

Three species of closely related woodpeckers (sapsuckers; Sphyrapicus) hybridize where they come into contact, presenting a rare ‘λ‐shape’ meeting of hybrid zones. Two of the three arms of this hybrid zone are located on either side of the Interior Plateau of British Columbia, Canada bordering the foothills of the Coast Mountains and the Rocky Mountains. The third arm is located in the eastern foothills of the Rocky Mountains. The zones of hybridization present high variability of phenotypes and alleles in relatively small areas and provide an opportunity to examine levels of reproductive isolation between the taxa involved. We examined phenotypes (morphometric traits and plumage) and genotypes of 175 live birds across the two hybrid zones. We used the Genotyping By Sequencing (GBS) method to identify 180 partially diagnostic single nucleotide polymorphisms (SNPs) to generate a genetic hybrid index (GHI) for each bird. Phenotypically diverged S. ruber and S. nuchalis are genetically closely related, while S. nuchalis and S. varius have similar plumage but are well separated at the genetic markers studied. The width of both hybrid zones is narrower than expected under neutrality, and analyses of both genotypes and phenotypes indicate that hybrids are rare in the hybrid zone. Rarity of hybrids indicates assortative mating and/or some form of fitness reduction in hybrids, which might maintain the species complex despite close genetic distance and introgression. These findings further support the treatment of the three taxa as distinct species.     

The importance of pre-mating barriers and the local demographic context for contemporary mating patterns in hybrid zones of Eucalyptus aggregata and Eucalyptus rubida

The frequency of hybridization in plants is context dependent and can be influenced by the local mating environment. We used progeny arrays and admixture and pollen dispersal analyses to assess the relative importance of pre‐mating reproductive barriers and the local demographic environment as explanations of variation in hybrid frequency in three mapped hybrid zones of Eucalyptus aggregata and E. rubida. A total of 731 open‐pollinated progeny from 36 E. aggregata maternal parents were genotyped using six microsatellite markers. Admixture analysis identified substantial variation in hybrid frequency among progeny arrays (0–76.9%). In one hybrid zone, hybrid frequency was related to pre‐mating barriers (degree of flowering synchrony) and demographic components of the local mating environment (decreasing population size, closer proximity to E. rubida and hybrid trees). At this site, average pollen dispersal distance was less and almost half (46%) of the hybrid progeny were sired by local E. rubida and hybrid trees. In contrast, at the other two sites, pre‐mating and demographic factors were not related to hybrid frequency. Compared to the first hybrid zone where most of the E. rubida (76%) and all hybrids flowered, in the remaining sites fewer E. rubida (22–41%) and hybrid trees (0–50%) flowered and their reproductive success was lower (sired 0–23% of hybrids). As a result, most hybrids were sired by external E. rubida/hybrids located at least 2–3 km away. These results indicate that although pre‐mating barriers and local demography can influence patterns of hybridization, their importance can depend upon the scale of pollen dispersal.     

Interploidy hybridization in sympatric zones: the formation of Epidendrum fulgens × E. puniceoluteum hybrids (Epidendroideae,Orchidaceae)

Interspecific hybridization is a primary cause of extensive morphological and chromosomal variation and plays an important role in plant species diversification. However, the role of interploidal hybridization in the formation of hybrid swarms is less clear. Epidendrum encompasses wide variation in chromosome number and lacks strong premating barriers, making the genus a good model for clarifying the role of chromosomes in postzygotic barriers in interploidal hybrids. In this sense, hybrids from the interploidal sympatric zone between E. fulgens (2n = 2x = 24) and E. puniceoluteum (2n = 4x = 56) were analyzed using cytogenetic techniques to elucidate the formation and establishment of interploidal hybrids. Hybrids were not a uniform group: two chromosome numbers were observed, with the variation being a consequence of severe hybrid meiotic abnormalities and backcrossing with E. puniceoluteum. The hybrids were triploids (2n = 3x = 38 and 40) and despite the occurrence of enormous meiotic problems associated with triploidy, the hybrids were able to backcross, producing successful hybrid individuals with broad ecological distributions. In spite of the nonpolyploidization of the hybrid, its formation is a long‐term evolutionary process rather than a product of a recent disturbance, and considering other sympatric zones in Epidendrum, these events could be recurrent.     

Variation in contact zone dynamics between two species of topminnows, Fundulus notatus and F. olivaceus, across isolated drainage systems

Spatially variable selection pressure within heterogeneous environments can result in the evolution of specialist phenotypes that facilitate co-occurrence of closely related species and limit genetic exchange. If divergent selection pressures maintain reproductive isolation, hybridization is expected to correlate with the strength of underlying ecological gradients and the traits shaped by adaptive processes. We sampled ten replicate topminnow (Fundulus olivaceus and Fundulus notatus) hybrid zones in isolated drainages throughout central and southern North America. In all drainages, species were distributed in an upstream–downstream manner with contact zones localized at confluences featuring abrupt shifts from tributary to river habitat. In two drainages, the typical up and downstream positions of species were reversed. Phenotype differences between the species reflect predicted selection differences along stream gradients. Downstream populations (lower food availability and greater predator pressure) generally showed larger investment in reproduction (higher gonadal somatic index), smaller body size and lower somatic condition compared to upstream populations. Phenotypic differences between the species in the two reversed drainages were consistent with convergence of life history traits in the respective habitats. Phenotypes of individuals of hybrid origin (F₁ hybrids or backcrosses) were not significantly different from the average of the two parental forms, though there were trends towards reduced fitness. The prevalence of hybridization among drainages ranged from no hybrids in two drainages to near random mating. The strongest correlates of hybridization rate among replicate hybrid zones were similarity in body shape and the homogeneity of habitat through tributary-river confluences. The two reversed orientation hybrid zones also exhibited high prevalence of hybrids suggesting that phenotypic convergence could lead to increased hybridization.     

Post‐zygotic isolation in cactophilic Drosophila: larval viability and adult life‐history traits of D. mojavensis/D. arizonae hybrids

Drosophila mojavensis and Drosophila arizonae are cactophilic flies that have been used extensively in speciation studies. Incomplete premating isolation, evidence of reinforcement, and a lack of recent introgression between these species point to a potentially important role for post‐zygotic isolating barriers in this system. Other than hybrid male sterility, however, post‐zygotic isolation between D. mojavensis and D. arizonae has received little attention. In this study, we examined viability and life‐history traits of D. mojavensis/D. arizonae F₁ hybrids from sympatric crosses. Specifically, we reared hybrids and purebreds on the natural host cacti of each parental species and compared viability, development time, thorax length, and desiccation resistance between hybrids and purebreds. Interestingly, hybrid females from both crosses performed similarly or even better than purebred females. In contrast, hybrid sons of D. arizonae mothers, in addition to being sterile, had shorter average thorax length than males of both parental species, and hybrid males from both crosses had substantially lower desiccation resistance than D. mojavensis males. The probable cost to hybridization for D. mojavensis females resulting from reduced desiccation resistance of hybrid sons may have been an important selective factor in the history of reinforcement for crosses involving these females.     

Clonal diversity,clonal persistence and rapid taxon replacement in natural populations of species and hybrids of the Daphnia longispina complex

Hybridization is common among cyclical parthenogens, especially in zooplankton species assemblages of the genus Daphnia. To explore hybridization dynamics and the extent of clonal diversity in the Daphnia longispina complex, we analysed population structure in eight permanent lakes. Based on 15 microsatellite loci, three major taxonomic units emerged: two species, D. galeata and D. longispina and their F1 hybrids, supported by factorial correspondence analysis and two Bayesian methods. At the same time, the detection of backcross classes differed between methods. Mean clonal diversity was lowest in the F1 hybrids, as expected from the high rate of asexual reproduction. Within taxa, replicated genotypes were of clonal origin, but clonal lineages persisted in subsequent years in only one of three resampled lakes. In another lake, the taxon composition changed from being dominated by hybrids to complete dominance by one parental taxon. Such a year‐to‐year taxon replacement has not been reported for the D. longispina complex before. Our data on this hybrid complex illustrate that high‐resolution genotyping is essential for the understanding of ecological and evolutionary outcomes of hybridization in partially clonal taxa.     

Inferring responses to climate warming from latitudinal pattern of clonal hybridization

Climate warming may affect reproductive isolation between sympatric sister species by modifying reproductive phenology or mate choice. This is expected to result in a latitudinal progression of hybridization in response to the shifting of environmental conditions. The fish species northern redbelly dace (Chrosomus eos) and finescale dace (C. neogaeus) display a wide sympatric distribution in North America. The asexual reproduction of their hybrids allows determining where and when hybridization occurred. The aim of this study was twofold: first, to assess whether temperature affected reproductive isolation, and second, whether the effects of climate warming resulted in a latitudinal progression of hybridization. We performed a 500 km latitudinal survey (51 sites) in southeastern Quebec (Canada) and determined the distribution of clonal hybrid lineages. Results revealed a total of 78 hybrid lineages, including 70 which originated locally. We detected a significant difference between the southern and northern range of the survey in terms of the proportion of sites harboring local hybrids (20/23 vs. 8/28 sites, respectively) and hybrid diversity (57 vs. 13 lineages, respectively). This confirmed that there was more frequent interspecific mating in the warmest sites. In the southern range, diversity of lineages and simulations suggest that hybridization first took place (>7,000 years) in sites characterized by a longer growing season, followed by northerly adjacent sites (ca. 3,500–5,000 years). Moreover, evidence of hybridization occurring in present‐day time was detected. This suggests that the current warming episode is going beyond the limits of the previous warmest period of the Holocene.     

Evolution of a hybrid zone of two willow species (Salix L.) in the European Alps analyzed by RAD-seq and morphometrics

Natural hybridization of plants can result in many outcomes with several evolutionary consequences, such as hybrid speciation and introgression. Natural hybrid zones can arise in mountain systems as a result of fluctuating climate during the exchange of glacial and interglacial periods, where species retract and expand their territories, resulting in secondary contacts. Willows are a large genus of woody plants with an immense capability of interspecific crossing. In this study, the sympatric area of two diploid sister species, S. foetida and S. waldsteiniana in the eastern European Alps, was investigated to study the genomic structure of populations within and outside their contact zone and to analyze congruence of morphological phenotypes with genetic data. Eleven populations of the two species were sampled across the Alps and examined using phylogenetic network and population genetic structure analyses of RAD Seq data and morphometric analyses of leaves. The results showed that a homoploid hybrid zone between the two species was established within their sympatric area. Patterns of genetic admixture in homoploid hybrids indicated introgression with asymmetric backcrossing to not only one of the parental species but also one hybrid population forming a separate lineage. The lack of F1 hybrids indicated a long-term persistence of the hybrid populations. Insignificant isolation by distance suggests that gene flow can act over large geographical scales. Morphometric characteristics of hybrids supported the molecular data and clearly separated populations of the parental species, but showed intermediacy in the hybrid zone populations with a bias toward S. waldsteiniana. The homoploid hybrid zone might have been established via secondary contact hybridization, and its establishment was fostered by the low genetic divergence of parental species and a lack of strong intrinsic crossing barriers. Incomplete ecological separation and the ability of long-distance dispersal of willows could have contributed to the spatial expansion of the hybrid zone.     

Patterns of cryptic hybridization revealed using an integrative approach: a case study on genets (Carnivora, Viverridae, Genetta spp.) from the southern African subregion

Recent years have seen the development of molecular‐based methodologies to investigate hybridization and its impact on the evolutionary process. However, morphological characterization of hybrid zones has only scantily been considered, especially in zootaxa. Thus, the level of congruence between molecular and morphological characters when attempting to detect hybrids remains a poorly tackled area. The genets (genus Genetta) provide an ideal case study for further investigation of the respective contribution of morphology and DNA in hybrid zone characterization because (1) their morphology has recently been exhaustively explored and (2) the existence of hybrid zones in southern Africa was proposed in the literature. We assessed levels of hybridization among the southern African genets, and questioned the role of ecological factors on the hybridization patterns detected. We used an integrative approach involving nine discrete morphological characters and a diagnostic discriminant function, geometric morphometrics and sequences of cytochrome b including collection specimens. The combination of independent materials allowed us to accurately reassess the level of hybridization in southern African genets, and revealed cryptic, interspecific gene flows. Morphology unambiguously detected a low number of G. maculata × G. tigrina hybrids and rejected the hypothesis of a large intergradation zone in KwaZulu‐Natal, thus supporting the species status of the two genets. Cytochrome b analyses revealed: (1) cryptic, massive hybridization between G. tigrina and the sympatric G. felina, and (2) a trace of reticulation (one sequence) between G. tigrina and the allopatric G. genetta. The type specimen of G. mossambica Matschie, 1902 is considered to be a morphological hybrid between G. maculata and G. angolensis. Remarkably, the morphological approaches (discrete characters and morphometrics) proved complementary to conclusions derived from cytochrome b sequences. Whilst morphometrics was generally unable to accurately identify all putative hybrids, this approach revealed diagnostic cranial shape differences between recognized species as well as the cryptic G. ‘letabae’ (included in the super‐species G. maculata). Morphometrics also confirmed the diagnostic value and age dependency of discrete characters. Our integrative approach appeared necessary to the detection of cryptic hybridizations and to the comprehensive characterization of hybrid zones. The recurrent detection of hybrids exhibiting tigrina‐like coat patterns may suggest (1) asymmetric hybridization of G. tigrina males to females of other species and (2) positive selection for tigrina‐like phenotype in South African habitats, but these hypotheses will have to be further tested using other sources of evidence. Despite the precise mosaic of hybrid zones identified in southern African genets, the environmental factors that shape patterns of distribution of hybrids remain unclear. Nevertheless, in the light of our range reassessment, it appears that seasonality of precipitation and periods of annual frost may play stringent roles in the distribution of genets. The complementarity of our results based on morphology and molecules is regarded as encouraging for the further development of integrative approaches in order to better understand the complex phenomena that underlie hybridization processes. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 86 , 11–33.     

Interspecific hybridization betweenDaphnia hyalina,D. galeata,andD. cucullata and seasonal abundances of these species and their hybrids

The three cladoceran speciesDaphnia hyalina, D. galeata, andD. cucullata frequently coexist in the lakes of northern Germany. Although there are some problems in distinguishing them morphologically, they are easily determined by gelelectrophoresis: each species carries a different allele at the glutamate oxaloacetate transaminase (GOT) locus. Animals morphologically intermediate between two species are heterozygous for the alleles carried by the species they resemble. This pattern is in agreement with the findings at other loci, where also diagnostic alleles exist. These findings are most easily explained by interspecific hybridization between the three species. No evidence is found for backcrosses involving hybrids ofD. cucullata, whereas some backcrosses betweenD. hyalina, D. galeata, and their hybrids are found in some lakes. In four lakes the seasonal abundances of the three species and their hybrids are determined.     

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).