Heterostyly accelerates diversification via reduced extinction in primroses.
ABSTRACT: The exceptional species diversity of flowering plants, exceeding that of their sister group more than 250-fold, is especially evident in floral innovations, interactions with pollinators and sexual systems. Multiple theories, emphasizing flower-pollinator interactions, genetic effects of mating systems or high evolvability, predict that floral evolution profoundly affects angiosperm diversification. However, consequences for speciation and extinction dynamics remain poorly understood. Here, we investigate trajectories of species diversification focusing on heterostyly, a remarkable floral syndrome where outcrossing is enforced via cross-compatible floral morphs differing in placement of their respective sexual organs. Heterostyly evolved at least 20 times independently in angiosperms. Using Darwin's model for heterostyly, the primrose family, we show that heterostyly accelerates species diversification via decreasing extinction rates rather than increasing speciation rates, probably owing to avoidance of the negative genetic effects of selfing. However, impact of heterostyly appears to differ over short and long evolutionary time-scales: the accelerating effect of heterostyly on lineage diversification is manifest only over long evolutionary time-scales, whereas recent losses of heterostyly may prompt ephemeral bursts of speciation. Our results suggest that temporal or clade-specific conditions may ultimately determine the net effects of specific traits on patterns of species diversification.
Project description:The loss of sexual recombination and segregation in asexual organisms has been portrayed as an irreversible process that commits asexually reproducing lineages to reduced diversification. We test this hypothesis by estimating rates of speciation, extinction, and transition between sexuality and functional asexuality in the evening primroses. Specifically, we estimate these rates using the recently developed BiSSE (Binary State Speciation and Extinction) phylogenetic comparative method, which employs maximum likelihood and Bayesian techniques. We infer that net diversification rates (speciation minus extinction) in functionally asexual evening primrose lineages are roughly eight times faster than diversification rates in sexual lineages, largely due to higher speciation rates in asexual lineages. We further reject the hypothesis that a loss of recombination and segregation is irreversible because the transition rate from functional asexuality to sexuality is significantly greater than zero and in fact exceeded the reverse rate. These results provide the first empirical evidence in support of the alternative theoretical prediction that asexual populations should instead diversify more rapidly than sexual populations because they are free from the homogenizing effects of sexual recombination and segregation. Although asexual reproduction may often constrain adaptive evolution, our results show that the loss of recombination and segregation need not be an evolutionary dead end in terms of diversification of lineages.
Project description:<h4>Background and aims</h4>Heterostyly is a floral polymorphism that has fascinated evolutionary biologists since Darwin's seminal studies on primroses. The main morphological characteristic of heterostyly is the reciprocal placement of anthers and stigmas in two distinct (distyly) floral morphs. Variation in the degree of intermorph sexual reciprocity is relatively common and known to affect patterns of pollen transfer within species. However, the partitioning of sexual organ reciprocity within and between closely related species remains unknown. This study aimed at testing whether intermorph sexual reciprocity differs within vs. between primrose species that hybridize in nature and whether the positions of sexual organs are correlated with other floral traits.<h4>Methods</h4>Six floral traits were measured in both floral morphs of 15 allopatric populations of Primula elatior, P. veris and P. vulgaris, and anther-stigma reciprocity was estimated within and between species. A combination of univariate and multivariate approaches was used to test whether positions of reproductive organs were less reciprocal between than within species, to assess correlations between sexual organ positions and other corolla traits, and to quantify differences between morphs and species.<h4>Key results</h4>The three species were morphologically well differentiated in most floral traits, except that P. veris and P. vulgaris did not differ significantly in sexual organ positions. Overall, lower interspecific than intraspecific sexual organ reciprocity was detected. This decrease was marked between P. elatior and P. vulgaris, intermediate and variable between P. elatior and P. veris, but negligible between P. veris and P. vulgaris.<h4>Conclusions</h4>Differences in anther and stigma heights between the analysed primrose species were of the same magnitude or larger than intraspecific differences that altered pollen flow within other heterostylous systems. Therefore, it is possible to suggest that considerable reductions of sexual organ reciprocity between species may lower interspecific pollen flow, with potential effects on reproductive isolation.
Project description:The interaction between floral traits and reproductive isolation is crucial to explaining the extraordinary diversity of angiosperms. Heterostyly, a complex floral polymorphism that optimizes outcrossing, evolved repeatedly and has been shown to accelerate diversification in primroses, yet its potential influence on isolating mechanisms remains unexplored. Furthermore, the relative contribution of pre- versus postmating barriers to reproductive isolation is still debated. No experimental study has yet evaluated the possible effects of heterostyly on pre- and postmating reproductive mechanisms. We quantify multiple reproductive barriers between the heterostylous Primula elatior (oxlip) and P. vulgaris (primrose), which readily hybridize when co-occurring, and test whether traits of heterostyly contribute to reproductive barriers in unique ways. We find that premating isolation is key for both species, while postmating isolation is considerable only for P. vulgaris; ecogeographic isolation is crucial for both species, while phenological, seed developmental, and hybrid sterility barriers are also important in P. vulgaris, implicating sympatrically higher gene flow into P. elatior. We document for the first time that, in addition to the aforementioned species-dependent asymmetries, morph-dependent asymmetries affect reproductive barriers between heterostylous species. Indeed, the interspecific decrease of reciprocity between high sexual organs of complementary floral morphs limits interspecific pollen transfer from anthers of short-styled flowers to stigmas of long-styled flowers, while higher reciprocity between low sexual organs favors introgression over isolation from anthers of long-styled flowers to stigmas of short-styled flowers. Finally, intramorph incompatibility persists across species boundaries, but is weakened in long-styled flowers of P. elatior, opening a possible backdoor to gene flow through intramorph pollen transfer between species. Therefore, patterns of gene flow across species boundaries are likely affected by floral morph composition of adjacent populations. To summarize, our study highlights the general importance of premating isolation and newly illustrates that both morph- and species-dependent asymmetries shape boundaries between heterostylous species.