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A compound hypothesis positing that self-fertilization is an evolutionary dead end conflates two distinct claims: the transition from outcrossing to selfing is unidirectional; and the diversification rate, or the balance of the speciation and extinction rate, is negative for selfing species. Both claims have enjoyed widespread informal support for decades, but have recently come under suspicion. Sources of data that apparently contradict strongly asymmetric mating system transitions often rely on statistical phylogenetic tests plagued by profound flaws. Although recently developed models mend preceding approaches, they have been employed sparingly, and many problems remain. Theoretical investigations, genetic data and applications of new phylogenetic methods provide indirect support for an association of selfing with negative diversification rates. We lack direct tests of reversals from selfing to outcrossing, and require data concerning the genetic basis and complexity of independently evolved outcrossing adaptations. The identification of the mechanisms that limit the longevity of selfing lineages has been difficult. Limitations may include brief and variable durations of selfing lineages, as well as ongoing difficulties in relating additive genetic and nucleotide variation. Furthermore, a common line of evidence for the stability of mixed mating – based simply on its frequent occurrence – is misleading. We make specific suggestions for research programs that aim to provide a richer understanding of mating system evolution and seriously challenge Stebbins' venerable hypothesis.

• Background The field of plant mating-system evolution has long been interested in understanding why selfing evolves from outcrossing. Many possible mechanisms drive this evolutionary trend, but most research has focused upon the transmission advantage of selfing and its ability to provide reproductive assurance when cross-pollination is uncertain. We discuss the shared conceptual framework of these ideas and their empirical support that is emerging from tests of their predictions over the last 25 years. • Scope These two hypotheses are derived from the same strategic framework. The transmission advantage hypothesis involves purely gene-level selection, with reproductive assurance involving an added component of individual-level selection. Support for both of these ideas has been garnered from population-genetic tests of their predictions. Studies in natural populations often show that selfing increases seed production, but it is not clear if this benefit is sufficient to favour the evolution of selfing, and the ecological agents limiting outcross pollen are often not identified. Pollen discounting appears to be highly variable and important in systems where selfing involves multiple floral adaptations, yet seed discounting has rarely been investigated. Although reproductive assurance appears likely as a leading factor facilitating the evolution of selfing, studies must account for both seed and pollen discounting to adequately test this hypothesis. • Conclusions The transmission advantage and reproductive assurance ideas describe components of gene transmission that favour selfing. Future work should move beyond their dichotomous presentation and focus upon understanding whether selection through pollen, seed or both explains the spread of selfing-rate modifiers in plant populations.

Baker's law refers to the tendency for species that establish on islands by long-distance dispersal to show an increased capacity for self-fertilization because of the advantage of self-compatibility when colonizing new habitat. Despite its intuitive appeal and broad empirical support, it has received substantial criticism over the years since it was proclaimed in the 1950s, not least because it seemed to be contradicted by the high frequency of dioecy on islands. Recent theoretical work has again questioned the generality and scope of Baker's law. Here, we attempt to discern where the idea is useful to apply and where it is not. We conclude that several of the perceived problems with Baker's law fall away when a narrower perspective is adopted on how it should be circumscribed. We emphasize that Baker's law should be read in terms of an enrichment of a capacity for uniparental reproduction in colonizing situations, rather than of high selfing rates. We suggest that Baker's law might be tested in four different contexts, which set the breadth of its scope: the colonization of oceanic islands, metapopulation dynamics with recurrent colonization, range expansions with recurrent colonization, and colonization through species invasions.

Because establishing a new population often depends critically on finding mates, individuals capable of uniparental reproduction may have a colonization advantage. Accordingly, there should be an over-representation of colonizing species in which individuals can reproduce without a mate, particularly in isolated locales such as oceanic islands. Despite the intuitive appeal of this colonization filter hypothesis (known as Baker’s law), more than six decades of analyses have yielded mixed findings. We assembled a dataset of island and mainland plant breeding systems, focusing on the presence or absence of self-incompatibility. Because this trait enforces outcrossing and is unlikely to re-evolve on short timescales if it is lost, breeding system is especially likely to reflect the colonization filter. We found significantly more self-compatible species on islands than mainlands across a sample of > 1500 species from three widely distributed flowering plant families (Asteraceae, Brassicaceae and Solanaceae). Overall, 66% of island species were self-compatible, compared with 41% of mainland species. Our results demonstrate that the presence or absence of self-incompatibility has strong explanatory power for plant geographical patterns. Island floras around the world thus reflect the role of a key reproductive trait in filtering potential colonizing species in these three plant families.

Self-compatibility and adaptations to self-fertilization are often found in plant populations at the periphery of species' ranges or on islands. Self-compatibility may predominate in these environments because it provides reproductive assurance when pollinators or availability of mates limits seed production. This possibility was studied in Leavenworthia alabamica, a flowering plant endemic to the southeastern United States. Populations at the center of the species' range retain sporophytic self-incompatibility, but peripheral populations are smaller, self-compatible, and have adaptations for self-fertilization. A reciprocal-transplant experiment was designed to test whether there is pollen limitation of seed set and to examine its strength in central and peripheral populations. Self-compatible genotypes produced more fruit and 17-22% more seed than self-incompatible genotypes in all environments, suggesting that the transition to self-compatibility may be favored by natural selection in all populations inhabited by L. alabamica. Sequence analyses demonstrated that two peripheral populations have 90-100% reductions in genetic variation, consistent with the effects of small population size or historical bottlenecks. Although pollen limitation of seed set occurs in all environments, self-compatibility may evolve at the periphery in L. alabamica because the benefits of reproductive assurance are influenced by population size or bottlenecks following extinction and colonization.

PREMISE OF THE STUDY: Direct tests of a species distribution model (SDM) were used to evaluate the hypothesis that the northern and southern edges of Mimulus bicolor's geographical range are limited by temperature and precipitation. METHODS: Climatic suitability was predicted using an SDM informed only by temperature and precipitation variables. These predictions were tested by growing plants in growth chambers with temperature and watering treatments informed by weather stations characteristic of environments at the geographic center, edges, and outside the range. An Aster analysis was used to assess whether treatments significantly affected lifetime flower production and to test for local adaptation. The relationship between climatic suitability and lifetime flower number in the growth chambers was also evaluated. KEY RESULTS: The temperature and watering treatments significantly affected lifetime flower number, although local adaptation was not detected. Flower production was significantly lower under the two edge treatments compared to the central treatment. While no flowers were produced under the beyond‐south treatments, flower production was greatest under the beyond‐north treatment. These results suggest a hard abiotic limit at the southern edge, and suitable temperature and precipitation conditions beyond the northern edge. While predicted climatic suitability was significantly lower at the range edges, there was no correlation between the climatic suitability of the weather stations’ locations and flower production. CONCLUSIONS: These results suggest that temperature and precipitation play a significant role in defining the distribution of M. bicolor, but also indicate that dispersal limitation or metapopulation dynamics are likely important factors restricting access to habitable sites beyond the northern range limit.

Colonization at expanding range edges often involves few founders, reducing effective population size. This process can promote the evolution of self‐fertilization, but implicating historical processes as drivers of trait evolution is often difficult and requires an explicit model of biogeographic history. In plants, contemporary limits to outcrossing are often invoked as evolutionary drivers of self‐fertilization, but historical expansions may shape mating system diversity, with leading‐edge populations evolving elevated selfing ability. In a widespread plant, Campanula americana, we identified a glacial refugium in the southern Appalachian Mountains from spatial patterns of genetic drift among 24 populations. Populations farther from this refugium have smaller effective sizes and fewer rare alleles. They also displayed elevated heterosis in among‐population crosses, reflecting the accumulation of deleterious mutations during range expansion. Although populations with elevated heterosis had reduced segregating mutation load, the magnitude of inbreeding depression lacked geographic pattern. The ability to self‐fertilize was strongly positively correlated with the distance from the refugium and mutation accumulation—a pattern that contrasts sharply with contemporary mate and pollinator limitation. In this and other species, diversity in sexual systems may reflect the legacy of evolution in small, colonizing populations, with little or no relation to the ecology of modern populations.

The ABO locus in humans is characterized by elevated heterozygosity and very similar allele frequencies among populations scattered across the globe. Using knowledge of ABO protein function, we generated a simple model of asymmetric negative frequency dependent selection and genetic drift to explain the maintenance of ABO polymorphism and its loss in human populations. In our models, regardless of the strength of selection, models with large effective population sizes result in ABO allele frequencies that closely match those observed in most continental populations. Populations must be moderately small to fall out of equilibrium and lose either the A or B allele (N(e) ≤ 50) and much smaller (N(e) ≤ 25) for the complete loss of diversity, which nearly always involved the fixation of the O allele. A pattern of low heterozygosity at the ABO locus where loss of polymorphism occurs in our model is consistent with small populations, such as Native American populations. This study provides a general evolutionary model to explain the observed global patterns of polymorphism at the ABO locus and the pattern of allele loss in small populations. Moreover, these results inform the range of population sizes associated with the recent human colonization of the Americas.

The northern fowl mite (NFM) Ornithonyssus sylviarum Canestrini and Fanzago is a blood-feeding ectoparasite found on many wild bird species and is a pest of poultry in the United States. It is unknown where NFM infestations of poultry originate, which has made it difficult to establish preventative biosecurity or effective control. We used microsatellite markers to evaluate genetic variation within and among NFM populations to determine routes of introduction onto farms and long-term persistence. We compared NFM from flocks of chickens (Gallus gallus) on different farms in California, Washington, and Georgia, and we compared NFM collected over a 5-yr interval. On three farms we collected NFM from chickens and house sparrows (Passer domesticus) nesting on each farm, which we used to assess movement between host species.There was strong genetic structure among mites from different poultry farms and low estimates of migration between farms. There were significant differences between mites on chickens and house sparrows on two farms where sparrows nested near flocks, indicating no exchange of mites. Only one farm showed evidence of NFM movement between chickens and sparrows.There was high genetic similarity between mites collected 5 yr apart on each of two farms, indicating that NFM infestations can persist for long periods.The genetic patterns did not reveal sources of NFM infestations on chicken farms.The data suggest that NFMs are strongly differentiated, which likely reflects periodic population declines with flock turnover and pesticide pressure.

Although selfing populations harbor little genetic variation limiting evolutionary potential, the causes are unclear. We experimentally evolved large, replicate populations of Mimulus guttatus for nine generations in greenhouses with or without pollinating bees and studied DNA polymorphism in descendants. Populations without bees adapted to produce more selfed seed yet exhibited striking reductions in DNA polymorphism despite large population sizes. Importantly, the genome-wide pattern of variation cannot be explained by a simple reduction in effective population size, but instead reflects the complicated interaction between selection, linkage, and inbreeding. Simulations demonstrate that the spread of favored alleles at few loci depresses neutral variation genome wide in large populations containing fully selfing lineages. It also generates greater heterogeneity among chromosomes than expected with neutral evolution in small populations. Genome-wide deviations from neutrality were documented in populations with bees, suggesting widespread influences of background selection. After applying outlier tests to detect loci under selection, two genome regions were found in populations with bees, yet no adaptive loci were otherwise mapped. Large amounts of stochastic change in selfing populations compromise evolutionary potential and undermine outlier tests for selection. This occurs because genetic draft in highly selfing populations makes even the largest changes in allele frequency unremarkable.