We present a new simple model for the evolution of premating reproductive isolation. Using this model we first analyze the level of genetic variability maintained by mutation in a large stable population. Then we consider the plausibility of the evolution of strong premating reproductive isolation after a founder event. We demonstrate that after a founder event a new adaptive combination of genes may rise to high frequencies in the presence of an old combination of genes. We compare the probabilities of speciation after a founder event with those in a stable population and with those when reproductive isolation is due to viability selection against hybrids. We argue that premating reproductive isolation is more efficient than postmating reproductive isolation in maintaining the integrity of sympatric species. This might have contributed to the pattern of stronger premating isolation than postmating isolation between closely related pairs of sympatric species.

Crosses have revealed the species‐specific, positively correlated intensities of paternally expressed growth enhancer (GE) and maternally expressed growth suppressor (GS), which serve as a reproductive isolation mechanism in many plants and animals. However, how this mechanism evolved has remained unanswered. A dynamic model shows that the conflict between paternally and maternally inherited genomes may drive them to an evolutionary “arms race” of their GE and GS productions, respectively. This results in paternally expressed GE and maternally expressed GS, and their evolutionarily stable intensities are both decreasing functions of species‐specific degree of paternity and GE and GS production costs, thereby establishing a mechanism for postzygotic isolation.

Ecological interactions and the natural selection they cause play a prominent causal role in biological diversification and speciation. As a discipline, ecological genetics integrates the two components of adaptive evolution (natural selection and genetic variability) to study the mechanisms of evolution. Ecological genetics is a fruitful approach to the study of how reproductive isolation can evolve under natural selection. The essence of this way of thinking and the ways in which it can be used to address persistent open questions in speciation are discussed.

An intriguing aspect of the current renaissance in investigations of the genetics of reproductive isolation is that it has been dominated by studies that resemble work done in the 1930s, 1940s, and 1950s. The dominant model organism (Drosophila), research approaches, and traits of interest (sterility and inviability of hybrids) all harken back to this earlier era. Herein, we explore the factors that led to a rebirth of interest in the genetics of reproductive isolation and to the adoption of the approaches of an earlier generation of biologists. At the same time, we appeal for more intensive investigations of traits that reproductively isolate closely related species, inclusion of a greater range of organisms in studies of reproductive isolation, and focus on a broader range of questions surrounding speciation. We end with a description of ongoing quantitative trait loci (QTL) studies of conspecific sperm precedence in the ground crickets Allonemobius fasciatus and Allonemobius socius. We have found several QTL with large effects on variance in patterns of sperm utilization in backcross females. Moreover, some QTL have an antagonistic effect on conspecific sperm, a finding that lends support to the hypothesis that rapid evolution of conspecific sperm precedence is a by‐product of sexual conflict.

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

Polyploid plants are typically geographically separated from their diploid progenitors, but it is rarely known whether this segregation is maintained by habitat differentiation or by selection against triploid hybrids. We tested for habitat differentiation between diploid and tetraploid populations of Galax urceolata in the southeastern United States by comparing the abundance and richness of vegetation associated with their respective habitats and testing for spatial autocorrelation in the distributions of diploid and tetraploid plants. Diploid and tetraploid habitats did not differ with respect to plant species richness. Herbaceous plants were 500% more common in tetraploid than diploid populations, while shrubs and trees were more common in diploid populations. Differences were found for the relative abundances of the most common species, with three species being significantly more prevalent in tetraploid than diploid populations. Spatial patchiness was detected for diploids and tetraploids, on a scale of 25 km. These results provide evidence for habitat differentiation, which may contribute to the maintenance of spatial separation between diploid and tetraploid G. urceolata.

Animal genitalia often show distinct developmental and evolutionary relationships with other parts of the body. Morphological observations of 29 sexually dimorphic and monomorphic beetle species in 16 genera of families Scarabaeidae and Lucanidae, Coleoptera, in 53 locations revealed that male genitalia size was consistently and distinctly less variable than that of other body parts within the same population, while it differentiated more readily among different populations than other body parts. The most noticeable genitalia size differentiation occurred in populations that coexisted with morphologically and ecologically similar congeneric species. Such differentiation may indicate selection for reproductive isolation. These characteristics of genitalia morphology may have been instrumental in generating the speciation pattern seen in most beetles.

To understand speciation, we first need to know what species are. Yet debates over species concepts have seemed endless, with little obvious relevance to the study of speciation. Recently, there has been progress in resolving these debates, favoring a lineage‐based, evolutionary species concept. This progress calls for reconsideration of the study of speciation. Traditional speciation research based on the biological species concept has led to great advances in understanding how nonallopatric speciation occurs and how species diverge and remain separate from each other. However, this research has neglected the question of how new species arise in the first place for the most common geographic mode (allopatric). A new and very different research program is needed to understand the ecological and evolutionary processes that split an ancestral species into new allopatric lineages. This research program will connect speciation to many other fundamental questions in evolutionary biology, ecology, biogeography, and conservation biology.

A central question in evolutionary biology is why animal lineages differ strikingly in rates and patterns of the evolution of reproductive isolation. Here, we show that the maximum genetic distance at which interspecific mammalian pregnancies yield viable neonates is significantly greater in clades with invasive (hemochorial) placentation than in clades with noninvasive (epitheliochorial or endotheliochorial) placentation. Moreover, sister species with invasive placentation exhibit higher allopatry in their geographic ranges, suggesting that formerly separated populations in mammals with this placental type fuse more readily on recontact. These differences are apparently driven by the stronger downregulation of maternal immune responses under invasive placentation, where fetal antigens directly contact the maternal bloodstream. Our results suggest that placental invasiveness mediates a major component of reproductive isolation in mammals.

Although predation is thought to affect species divergence, the effects of predator‐mediated natural selection on species divergence and in nonadaptive radiations have seldom been studied. Wing melanization in Calopteryx damselflies has important functions in sexual selection and interspecific interactions and in species recognition. The genus Calopteryx and other damselfly genera have also been put forward as examples of radiations driven by sexual selection. We show that avian predation strongly affects natural selection on wing morphology and male wing melanization in two congeneric and sympatric species of this genus (Calopteryx splendens and Calopteryx virgo). Predation risk was almost three times higher for C. virgo, which has an exaggerated degree of wing melanization, than it was for the less exaggerated, sympatric congener C. splendens. Selective predation on the exaggerated species C. virgo favored a reduction and redistribution of the wing melanin patch. There was evidence for nonlinear selection involving wing patch size, wing patch darkness, and wing length and width in C. splendens but weaker nonlinear selection on the same trait combinations in C. virgo. Selective predation could interfere with species divergence by sexual selection and may thus indirectly affect male interspecific interactions, reproductive isolation, and species coexistence in this genus.

Various evolutionary forces may shape the evolution of traits that influence the mating decisions of males and females. Phenotypic traits that males and females use to judge the species identify of potential mates should evolve in a punctuated fashion, changing significantly at the time of speciation but changing little between speciation events. In contrast, traits experiencing sexual selection or sexually antagonistic interactions are generally expected to change continuously over time because of the directional selection pressures imposed on one sex by the actions of the other. To test these hypotheses, we used spherical harmonic representations of the shapes of male mating structures in reconstructions of the evolutionary tempo of these structures across the history of the Enallagma damselfly clade. Our analyses show that the evolution of these structures is completely consistent with a punctuated model of evolutionary change and a constant evolutionary rate throughout the clade’s history. In addition, no interpopulation variation in shape was detected across the range of one species. These results indicate that male mating structures in this genus are used primarily for identifying the species of potential mates and experience little or no selection from intraspecific sexual selection or sexual antagonism. The implications of these results for speciation are discussed.

Speciation with gene flow may be driven by a combination of positive assortative mating and disruptive selection, particularly if selection and assortative mating act on the same trait, eliminating recombination between ecotype and mating type. Phenotypically unimodal populations of threespine stickleback (Gasterosteus aculeatus) are commonly subject to disruptive selection due to competition for alternate prey. Here we present evidence that stickleback also exhibit assortative mating by diet. Among‐individual diet variation leads to variation in stable isotopes, which reflect prey use. We find a significant correlation between the isotopes of males and eggs within their nests. Because egg isotopes are derived from females, this correlation reflects assortative mating between males and females by diet. In concert with disruptive selection, this assortative mating should facilitate divergence. However, the stickleback population remains phenotypically unimodal, highlighting the fact that assortative mating and disruptive selection do not guarantee evolutionary divergence and speciation.

The evolution of viviparity increases the potential for genomic conflicts between mothers and offspring over the level of maternal investment. The viviparity‐driven‐conflict hypothesis predicts that such conflicts will drive the evolution of asymmetrical reproductive isolation between populations with divergent mating systems. We tested this hypothesis using crosses between populations of a poeciliid fish that differ in their level of polyandry. Our results support the prediction of an asymmetry in the rate of spontaneous abortion in reciprocal crosses, with the highest rate occurring in crosses between females from a relatively monandrous population and males from a relatively polyandrous population. The patterns of offspring size were not consistent with the pattern predicted by the viviparity‐driven‐conflict hypothesis: crosses between a monandrous female and a polyandrous male did not produce larger offspring than the reciprocal cross. This discrepancy was due to the presence of an effect of the maternal population on offspring size: polyandrous females produced larger offspring than monandrous females. In addition, offspring size was positively correlated with maternal size in crosses involving a polyandrous male. We discuss these results in light of models for intra‐ and intergenomic epistasis and the rapid origin of asymmetric reproductive isolation in viviparous taxa.

Gene flow can limit local adaptation and speciation. The outcome of breeding between populations determines the effectiveness of migration and the extent of gene flow. In crosses between populations, it is possible that some traits may indicate isolation and others may not. I measured the rate of successful hand pollination and the fruit production of the resulting hybrid progeny of crosses within and between six populations of the selfing annual Diodia teres. I chose two populations from each of three habitat types to examine evidence for reproductive isolation and heterosis between populations from different habitats. There was postmating/prezygotic isolation in crosses between populations from different habitats and heterosis for fruit production in the F₂ progeny of these crosses, as well as crosses between populations from the same habitat type. Specific pairs of populations showed postmating/prezygotic isolation, but there was heterosis for fruit production in some hybrids. Populations that develop postmating/prezygotic isolation may not diverge further if heterosis in the resulting offspring leads to increased gene flow. The heterosis suggests fixed genetic load within some populations, which may be common in selfing species and may limit local adaptation and speciation.

A central goal in evolutionary biology is to elucidate general mechanisms and patterns of species divergence. The viviparity‐driven conflict (VDC) hypothesis posits that intense mother‐embryo conflict associated with viviparity drives rapid reproductive isolation among viviparous species, is intensified by multiple paternity, and reduces female reliance on precopulatory cues in mate choice. We tested these predictions using comparisons of oviparous and viviparous fishes. Consistent with the VDC hypothesis, we found that, relative to oviparous species, only closely related viviparous fishes are known to hybridize. Also in support of the VDC hypothesis, we found that (1) elaborate male sexual ornamentation may be more common in viviparous species with relatively low levels of maternal provisioning of embryos compared with those with high levels of provisioning and (2) the degree of multiple paternity is higher in viviparous species than in oviparous species. In contrast to a prediction of the VDC hypothesis, we found no relationship between the degree of multiple paternity and elaborate male sexual ornamentation, although statistical power was quite low for this test. Whereas overall our results strongly support the central tenet of the VDC hypothesis—that reproductive mode affects rates of evolution of reproductive isolation and the strength of sexual selection—they cannot rule out two alternative models we propose that may also explain the observed patterns.

As reflected in the title of his masterwork On the Origin of Species, Darwin proposed that adaptation is the primary mechanism of speciation. On this, Darwin was criticized for his neglect of reproductive isolation, his lack of appreciation for the role of geographic barriers, his failure to distinguish varieties from species, and his typological species concept. Two developments since Darwin, the biological species concept of Ernst Mayr and the methods of Coyne and Orr for estimating the contribution of different barriers to the total reproductive isolation, provide a framework for reconciling Darwin’s view on the primacy of adaptation in speciation with later proposals that emphasize reproductive isolation. A review of the few studies that have estimated the contributions of multiple isolating barriers suggests that habitat isolation and other barriers that operate before hybrid formation are much stronger than intrinsic postzygotic isolation. In light of these data, I suggest that Darwin’s focus on adaptation in the origin of species was essentially correct, a conclusion that calls for future studies that explore the links between adaptation and speciation, in particular, ecogeographic isolating barriers that result from adaptive divergence in habitat use. The recent revival in thinking about ecological factors and adaptive divergence in the origin of species echoes Darwin’s much‐criticized “principle of divergence” and suggests that the emerging views from today’s naturalists are not so different from those espoused by Darwin some 150 years ago.

Assortative mating may result from intrinsic individual mating preferences or from assortment traits not requiring expression of preferences. Assortment traits are phenotypes expressed in both sexes that enhance the probability of encountering individuals possessing similar trait values. In the noctuid moth Spodoptera frugiperda, it has been suggested that nonrandom mating between two host strains is caused by a temporal assortment trait—that is, differential timing of calling and copulation during the night. By experimental manipulation of this trait in controlled mate-choice experiments, we investigated whether mating by same-strain individuals is enhanced mainly by the allochronic shift of mating activity or is also affected by time-independent intrinsic mating preferences. The observed patterns suggest that nonrandom mating between the two host strains in the laboratory is shaped by an interaction of both effects that is dominated by mating preferences during the first encounter night. This interaction changes over time as the preferences become weaker on subsequent nights. Males were less restricted than females with regard to both the time shift in mating activity and mate preferences. Although the nature of the mate-preference mechanism remains elusive, its restriction to females suggests that male-produced close-range pheromones emitted during courtship play a role.

Ecological divergence and selection for novel adaptations to new habitats have been theoretically proposed to play important roles in promoting homoploid hybrid speciation (HHS). The successful establishment of Pinus densata on the Tibetan Plateau is one of the few known examples of HHS. In this study, we carried out extensive field expeditions to obtain representative coverage of occurrence sites of P. densata and its two putative parents. We then applied a series of geographic information system–based analyses to define the patterns of environmental variation within and among the three pine species, to remove potentially confounding effects of spatial autocorrelation in the environmental data due to allopatric ranges, and to build species distribution models. All results consistently indicated that the ecological preferences of P. densata and its parental species have diverged, and they identified candidate ecological factors associated with habitat-specific adaptation. Projections from niche modeling indicated that P. densata could extend across a vast range along the parallel valley systems of the southeastern Tibetan Plateau. Our findings provide evidence of a distinct niche shift in P. densata and support the hypothesis that local adaptation and geographic isolation help maintain and reinforce between-species differences and reproductive isolation in the species complex.

Range expansions are critical to renewed bouts of allopatric or parapatric speciation. Limits on range expansions—and, by implication, speciation—include dispersal ability and permeability of geographical barriers. In addition, recently diverged taxa may interfere with each other, preventing mutual expansion of each other’s range into sympatry, because reproductive isolation is incomplete and/or ecological competition particularly strong. On the basis of geographical distributions and mitochondrial DNA phylogenetic information for 418 recently diverged species of New World birds, we estimate that secondary sympatry takes on the order of millions of years following population splitting and hence could impose an important limit on the rate of range expansion, thereby limiting further rounds of species formation. Average rates of achievement of sympatry have been faster in the temperate region (we estimate 1.7 million years to sympatry at 60°) than in the tropics (3.2 million years to sympatry at the equator). Evidence from the ages of species with hybrid zones implies that one factor associated with the slowed sympatry in the tropics is the rate of accumulation of reproductive isolation.

In addition to the observed high diversity of species in the tropics, divergence among populations of the same species exists over short geographic distances in both phenotypic traits and neutral genetic markers. Divergence among populations suggests great potential for the evolution of reproductive isolation and eventual speciation. In birds, song can evolve quickly through cultural transmission and result in regional dialects, which can be a critical component of reproductive isolation through variation in female preference. We examined female and male behavioral responses to local and nonlocal dialects in two allopatric populations of rufous-collared sparrows (Zonotrichia capensis) in the Andes Mountains of Ecuador. Here we show that female sparrows prefer their natal song dialect to the dialect of an allopatric population that is just 25 km away and separated by an unsuitable higher-elevation habitat (pass of 4,200 m), thus providing evidence of prezygotic reproductive isolation among populations. Males showed similar territorial responses to all conspecific dialects with no consistent difference with respect to distance, making male territoriality uninformative for estimating reproductive isolation. This study provides novel evidence for culturally based prezygotic isolation over very short distances in a tropical bird.