Divergent natural selection drives the evolution of reproductive isolation in an Australian wildflower

Ecological speciation occurs when reproductive isolation evolves between populations adapting to contrasting environments. A key prediction of this process is that the fitness of hybrids between divergent populations should be reduced in each parental environment as a function of the proportion of local genes they carry, a process resulting in ecologically dependent reproductive isolation (RI). To test this prediction, we use reciprocal transplant experiments between adjacent populations of an Australian wildflower, Senecio lautus, at two locations to distinguish between ecologically dependent and intrinsic genetic reproductive barriers. These barriers can be distinguished by observing the relative fitness of reciprocal backcross hybrids, as they differ in the contribution of genes from either parent while controlling for any intrinsic fitness effects of hybridization. We show ecologically dependent fitness effects in establishment and survival of backcrosses in one transplant experiment, and growth performance in the second transplant experiment. These results suggest natural selection can create strong reproductive barriers that maintain differentiation between populations with the potential to interbreed, and implies a significant role for ecology in the evolutionary divergence of S. lautus.     

Ecologically dependent and intrinsic genetic signatures of postzygotic isolation between sympatric host races of the leaf beetle Lochmaea capreae

The fitness of hybrids might be compromised as a result of intrinsic isolation and/or because they fall between ecological niches due to their intermediate phenotypes (“extrinsic isolation”). Here, we present data from several crosses (parental crosses, F1, F2, and backcrosses) between the two host races of Lochmaea capreae on willow and birch to test for extrinsic isolation, intrinsic isolation, and environmentally dependent genetic incompatibilities. We employed a reciprocal transplant design in which offspring were raised on either host plant and their survival was recorded until adulthood. We also applied joint‐scaling analysis to determine the genetic architecture of hybrid inviability. The relative fitness of the backcrosses switched between environments; furthermore, the additive genetic–environment interaction was detected as the strongest effect in our analysis. These results provide strong evidence that divergent natural selection has played a central role in the evolution of hybrid dysfunction between host races. Joint‐scaling analysis detected significant negative epistatic effects that are most evident in the poor performance of F2‐hybrids on willow, indicating signs of intrinsic isolation. We did not find any evidence that genetic incompatibilities are manifested independently of environmental conditions. Our findings suggest the outcome of natural hybridization between these host races is mainly affected by extrinsic isolation and a weak contribution of intrinsic isolation.     

Genetic incompatibilities in killifish and the role of environment

Measuring reproductive isolation across multiple generations and environments is a key endeavor in speciation research because it indicates which isolating barriers currently prevent introgression and the extent to which they are intrinsic versus environmentally dependent. Here, I present data from several crosses (parental crosses, F1s, F2s, back-crosses) between two species of killifish (Lucania goodei and L. parva) that have diverged along a salinity gradient (L. goodei--freshwater, L. parva--euryhaline). Offspring were raised under high and low salinity to test for (1) extrinsic isolation, (2) intrinsic isolation manifested through genetic incompatibilities, and (3) environmentally dependent genetic incompatibilities. I found evidence for both intrinsic and extrinsic isolation, but no evidence for environmentally dependent genetic incompatibilities. The presence of extrinsic and intrinsic isolation varied among fitness measures, and all forms of reproductive isolation were asymmetric. Early egg survival was independent of salinity, but demonstrated pronounced intrinsic isolation. Both extrinsic and intrinsic isolation existed for egg hatching and survival of fry to the eating stage. Unfortunately, the order in which extrinsic and intrinsic isolation arose is unresolved. Understanding the extent to which adaptation to salinity creates multiple forms of reproductive isolation is critical for understanding diversification in many fish taxa.     

A test of ecologically dependent postmating isolation between sympatric sticklebacks

Ecological speciation occurs when reproductive isolation evolves ultimately as a result of divergent natural selection between populations inhabiting different environments or exploiting alternative resources. I tested a prediction of the ecological model concerning the fitness of hybrids between two young, sympatric species of threespine sticklebacks (Benthics and Limnetics). The two species are ecologically and morphologically divergent: the Benthic is adapted to feeding on invertebrates in the littoral zone of the lake whereas the Limnetic is adapted to feeding on zooplankton in the open water. The growth rate of two types of hybrids, the Benthic backcross and the Limnetic backcross, as well as both parent species, was evaluated in enclosures in both parental habitats in the lake. The use of backcrosses is ideal because a comparison of their growth rates in the two habitats estimates an ecologically dependent component of their fitness while controlling for any intrinsic genetic incompatibilities that may exist between the Benthic and Limnetic genomes. The backcross results revealed a striking pattern of ecological dependence: in the littoral zone, Benthic backcrosses grew at approximately twice the rate of Limnetic backcrosses, while in the open water, Limnetic backcrosses grew at approximately twice the rate of Benthic backcrosses. Such a reversal of relative fitness of the two cross-types in the two environments provides strong evidence that divergent natural selection has played a central role in the evolution of postmating isolation between Benthics and Limnetics. Although the rank order of growth rates of all cross-types in the littoral zone was Benthic > Benthic backcross > Limnetic backcross > Limnetic, neither backcross differed significantly from the parent from which it was mainly derived. Implications of this result are discussed in terms of ecological speciation and possible introgressive hybridization between the species. Results in the open water were less clear and were not fully consistent with the ecological model of speciation, mainly as a result of the low growth rate of Limnetics. However, analysis of the diet of the fish in the open water suggests that these enclosures may not have been fully successful at replicating the food regimes characteristic of this habitat.     

Diversification across a heterogeneous landscape

Adaptation to contrasting environments across a heterogeneous landscape favors the formation of ecotypes by promoting ecological divergence. Patterns of fitness variation in the field can show whether natural selection drives local adaptation and ecotype formation. However, to demonstrate a link between ecological divergence and speciation, local adaptation must have consequences for reproductive isolation. Using contrasting ecotypes of an Australian wildflower, Senecio lautus in common garden experiments, hybridization experiments, and reciprocal transplants, we assessed how the environment shapes patterns of adaptation and the consequences of adaptive divergence for reproductive isolation. Local adaptation was strong between ecotypes, but weaker between populations of the same ecotype. F1 hybrids exhibited heterosis, but crosses involving one native parent performed better than those with two foreign parents. In a common garden experiment, F2 hybrids exhibited reduced fitness compared to parentals and F1 hybrids, suggesting that few genetic incompatibilities have accumulated between populations adapted to contrasting environments. Our results show how ecological differences across the landscape have created complex patterns of local adaptation and reproductive isolation, suggesting that divergent natural selection has played a fundamental role in the early stages of species diversification.     

No evidence of intrinsic reproductive isolation between two reciprocally non-monophyletic,ecologically differentiated mountain plants at an early stage of speciation

Adaptation to dissimilar habitats can trigger phenotypic and genetic differences between populations, which may, in the absence of gene flow, ultimately lead to ecological speciation. Reproductive isolation of diverging populations is a critical step at the onset of speciation. An excellent example for exploring the extent of reproductive isolation at early stages of speciation is provided by Heliosperma pusillum and H. veselskyi (Caryophyllaceae), two reciprocally non-monophyletic, ecologically differentiated species from the Alps. Interspecific gene flow—as revealed by recent genetic studies—is rare even between geographically close populations. Cross pollinations and fitness experiments revealed no evidence of intrinsic reproductive barriers, since fitness parameters measured under uniform conditions were not lower in inter- than in intraspecific crosses. Further, morphometric analyses of the offspring clearly showed that the differentiation of parental species is heritable. As parental phenotypes are likely adaptive, the intermediate morphology of hybrids may lead to reduced hybrid fitness in parental habitats. Altogether, H. pusillum and H. veselskyi provide an increasingly well characterised model system offering exciting insights into early stages of ecological speciation.     

Lifetime fitness in two generations of Ipomopsis hybrids

Various models purporting to explain natural hybrid zones make different assumptions about the fitness of hybrids. One class of models assumes that hybrids have intrinsically low fitness due to genetic incompatibilities, whereas other models allow hybrid fitness to vary across natural environments. We used the intrinsic rate of increase to assess lifetime fitness of hybrids between two species of montane plants Ipomopsis aggregata and Ipomopsis tenuituba planted as seed into multiple field environments. Because fitness is predicted to depend upon genetic composition of the hybrids, we included F1 hybrids, F2 hybrids, and backcrosses in our field tests. The F2 hybrids had female fitness as high, or higher, than expected under an additive model of fitness. These results run counter to any model of hybrid zone dynamics that relies solely on intrinsic nuclear genetic incompatibilities. Instead, we found that selection was environmentally dependent. In this hybrid zone, cytoplasmic effects and genotype-by-environment interactions appear more important in lowering hybrid fitness than do intrinsic genomic incompatibilities between nuclear genes.     

Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities

Despite its role in homogenizing populations, hybridization has also been proposed as a means to generate new species. The conceptual basis for this idea is that hybridization can result in novel phenotypes through recombination between the parental genomes, allowing a hybrid population to occupy ecological niches unavailable to parental species. Here we present an alternative model of the evolution of reproductive isolation in hybrid populations that occurs as a simple consequence of selection against genetic incompatibilities. Unlike previous models of hybrid speciation, our model does not incorporate inbreeding, or assume that hybrids have an ecological or reproductive fitness advantage relative to parental populations. We show that reproductive isolation between hybrids and parental species can evolve frequently and rapidly under this model, even in the presence of substantial ongoing immigration from parental species and strong selection against hybrids. An interesting prediction of our model is that replicate hybrid populations formed from the same pair of parental species can evolve reproductive isolation from each other. This non-adaptive process can therefore generate patterns of species diversity and relatedness that resemble an adaptive radiation. Intriguingly, several known hybrid species exhibit patterns of reproductive isolation consistent with the predictions of our model.     

ECOLOGICAL SPECIATION IN STICKLEBACKS: ENVIRONMENT-DEPENDENT HYBRID FITNESS

“Ecological” speciation occurs when reproductive isolation evolves as a consequence of divergent selection between populations exploiting different resources or environments. We tested this hypothesis of speciation in a young stickleback species pair by measuring the direct contribution of ecological selection pressures to hybrid fitness. The two species (limnetic and benthic) are strongly differentiated morphologically and ecologically, whereas hybrids are intermediate. Fitness of hybrids is high in the laboratory, especially F₁ and F₂ hybrids (backcrosses may show some breakdown). We transplanted F₁ hybrids to enclosures in the two main habitats in the wild to test whether the distribution of resources available in the environment generates a hybrid disadvantage not detectable in the laboratory. Hybrids grew more slowly than limnetics in the open water habitat and more slowly than benthics in the littoral zone. Growth of F₁ hybrids was inferior to the average of the parent species across both habitats, albeit not significantly. The contrast between laboratory and field results supports the hypothesis that mechanisms of F₁ hybrid fitness in the wild are primarily ecological and do not result from intrinsic genetic incompatibilities. Direct selection on hybrids contributes to the maintenance of sympatric stickleback species and may have played an important role in their origin.     

Immigrant inviability produces a strong barrier to gene flow between parapatric ecotypes of Senecio lautus

Speciation proceeds when gene exchange is prevented between populations. Determining the different barriers preventing gene flow can therefore give insights into the factors driving and maintaining species boundaries. These reproductive barriers may result from intrinsic genetic incompatibilities between populations, from extrinsic environmental differences between populations, or a combination of both mechanisms. We investigated the potential barriers to gene exchange between three adjacent ecotypes of an Australian wildflower to determine the strength of individual barriers and the degree of overall isolation between populations. We found almost complete isolation between the three populations mainly due to premating extrinsic barriers. Intrinsic genetic barriers were weak and variable among populations. There were asymmetries in some intrinsic barriers due to the origin of cytoplasm in hybrids. Overall, these results suggest that reproductive isolation between these three populations is almost complete despite the absence of geographic barriers, and that the main drivers of this isolation are ecologically based, consistent with the mechanisms underlying ecological speciation.