Weak response to selection on stigma-anther distance in a primarily selfing population of yellow monkeyflower.

Stebbins hypothesized that selfing lineages are evolutionary dead ends because they lack adaptive potential. While selfing populations often possess limited nucleotide variability compared with closely related outcrossers, reductions in the genetic variability of quantitative characters remain unclear, especially for key traits determining selfing rates. Yellow monkeyflower (Mimulus guttatus) populations generally outcross and maintain extensive quantitative genetic variation in floral traits. Here, we study the Joy Road population (Bodega Bay, CA, USA) of M. guttatus, where individuals exhibit stigma-anther distances (SAD) typical of primarily selfing monkeyflowers. We show that this population is closely related to nearby conspecifics on the Pacific Coast with a modest 33% reduction in genome-wide variation compared with a more highly outcrossing population. A five-generation artificial selection experiment challenged the hypothesis that the Joy Road population harbours comparatively low evolutionary potential in stigma-anther distance, a critical determinant of selfing rate in Mimulus. Artificial selection generated a weak phenotypic response, with low realized heritabilities (0.020-0.028) falling 84% below those measured for floral characters in more highly outcrossing M. guttatus. These results demonstrate substantial declines in evolutionary potential with a transition toward selfing. Whether these findings explain infrequent reversals to outcrossing or general limits on adaptation in selfers requires further investigation.

Pollinator loss causes rapid adaptive evolution of selfing and dramatically reduces genome-wide genetic variability.

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.

Hybrid breakdown is elevated near the historical cores of a species' range.

New species form when they become reproductively isolated. A classic model of speciation posits that derived mutations appear in isolated populations and reduce fitness when combined in hybrids. While these Bateson-Dobzhansky-Muller incompatibilities are known to accumulate as populations diverge over time, they may also reflect the amount of standing genetic variation within populations. We analysed the fitness of F2 hybrids in crosses between 24 populations of a plant species (Campanula americana) with broad variation in standing genetic variation and genetic differentiation driven by post-glacial range expansions. Hybrid breakdown varied substantially and was strongest between populations near the historical cores of the species range where within-population genetic diversity was high. Nearly half of the variation in hybrid breakdown was predicted by the combined effects of standing genetic variation within populations, their pairwise genetic differentiation and differences in the climates they inhabit. Hybrid breakdown was enhanced between populations inhabiting distinct climates, likely reflecting local adaptation. Results support that the mutations causing hybrid breakdown, the raw material for speciation, are more common in long-inhabited areas of the species range. Genetic diversity harboured in refugial areas is thus an important source of incompatibilities critical to the speciation process.

Selfing rate variation within species is unrelated to life-history traits or geographic range position.

PREMISE: In plants, populations and species vary widely along the continuum from outcrossing to selfing. Life-history traits and ecological circumstances influence among-species variation in selfing rates, but their general role in explaining intraspecific variation is unknown. Using a database of plant species, we test whether life-history traits, geographic range position, or abundance predict selfing rate variation among populations. METHODS: We identified species where selfing rates were estimated in at least three populations at known locations. Two key life-history traits (generation time and growth form) were used to predict within-species selfing rate variation. Populations sampled within a species' native range were assessed for proximity to the nearest edge and abundance. Finally, we conducted linear and segmented regressions to determine functional relationships between selfing rate and geographic range position within species. RESULTS: Selfing rates for woody species varied less than for herbs, which is explained by the lower average selfing rate of woody species. Relationships between selfing and peripherality or abundance significantly varied among species in their direction and magnitude. However, there was no general pattern of increased selfing toward range edges. A power analysis shows that tests of this hypothesis require studying many (i.e., 40+) populations. CONCLUSIONS: Intraspecific variation in plant mating systems is often substantial yet remains difficult to explain. Beyond sampling more populations, future tests of biogeographic hypotheses will benefit from phylogeographic information concerning specific range edges, the study of traits influencing mating system (e.g., herkogamy), and measures of abundance at local scales (e.g., population density).

Floral traits differentiate pollination syndromes and species but fail to predict the identity of floral visitors to Castilleja.

PREMISE: Animal pollination is critical to plant reproduction and may cause convergent evolution of pollination syndromes. Pollination syndromes in Castilleja have been distinguished based on floral traits and historical observations of floral visitors. Here we addressed these questions: (1) Can pollination syndromes be distinguished using floral morphological traits or volatile organic compound emissions? (2) Is there significant variation in floral traits within a pollination syndrome at the level of populations or species? (3) Do pollination syndromes predict the most frequent floral visitor to Castilleja? METHODS: Floral traits and visitation were measured for five co-occurring Castilleja species (C. applegatei, C. linariifolia, C. miniata, C. nana, and C. peirsonii), representing three pollination syndromes (bee, fly, and hummingbird), at four sites in the Sierra Nevada Mountains. We used nonmetric multidimensional scaling (NMDS) and multiple linear regressions to address key questions in the differentiation of Castilleja and floral visitors. RESULTS: Our analyses revealed that both morphological traits and floral VOCs can be used to distinguish between some pollination syndromes and Castilleja species. Morphological traits defined pollination syndromes reliably, but within the hummingbird syndrome, there was also significant variation among populations and species. Pollination syndrome was a poor predictor of visitors to Castilleja. CONCLUSIONS: Floral trait differentiation among Castilleja individuals reflects both taxonomy and pollination syndromes. Differentiation was generally more evident in morphological traits compared to VOCs. Furthermore, a priori notions of pollination syndromes in this system are overly simplistic and fail to predict which animals most frequently visit Castilleja in natural populations.

Westward range expansion from middle latitudes explains the Mississippi River discontinuity in a forest herb of eastern North America.

It is often expected that temperate plants have expanded their geographical ranges northward from primarily southern refugia. Evidence for this hypothesis is mixed in eastern North American species, and there is increasing support for colonization from middle latitudes. We studied genome-wide patterns of variation in RADseq loci to test hypotheses concerning range expansion in a North American forest herb (Campanula americana). First, spatial patterns of genetic differentiation were determined. Then phylogenetic relationships and divergence times were estimated. Spatial signatures of genetic drift were also studied to identify the directionality of recent range expansion and its geographical origins. Finally, spatially explicit scenarios for the spread of plants across the landscape were compared, using variation in the population mutation parameter and Tajima's D. We found strong longitudinal subdivision, with populations clustering into groups west and east of the Mississippi River. While the southeastern region was probably part of a diverse Pleistocene refugium, there is little evidence that range expansion involved founders from these southern locales. Instead, declines in genetic diversity and the loss of rare alleles support a westward colonization wave from a middle latitude refugium near the southern Appalachian Mountains, with subsequent expansion from a Pleistocene staging ground in the Mississippi River Valley (0.51-1.27 million years ago). These analyses implicate stepping stone colonization from middle latitudes as an important mechanism of species range expansion in eastern North America. This study further demonstrates the utility of population genetics as a tool to infer the routes travelled by organisms during geographical range expansion.

Genetic Structure of Northern Fowl Mite (Mesostigmata: Macronyssidae) Populations Among Layer Chicken Flocks and Local House Sparrows (Passeriformes: Passeridae).

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.

Selfing ability and drift load evolve with range expansion.

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.

Pollen limitation and autonomous selfing ability interact to shape variation in outcrossing rate across a species range.

PREMISE: Hermaphroditic plants commonly reproduce through a mixture of selfing and outcrossing. The degree to which outcrossing rates reflect the availability of outcross pollen, genetic differentiation in the ability to autonomously self-fertilize, or both is often unclear. Despite the potential for autonomy and the pollination environment to jointly influence outcrossing, this interaction is rarely studied. METHODS: We reviewed studies from the literature that tested whether the pollination environment or floral traits that cause autonomous selfing predict variation in outcrossing rate among populations. We also measured outcrossing rates in 23 populations of Campanula americana and examined associations with the pollination environment, autonomy, and their interaction. RESULTS: Our review revealed that traits that facilitate selfing were often negatively associated with outcrossing rates whereas most aspects of the pollination environment poorly predicted outcrossing. Populations of C. americana varied from mixed mating to highly outcrossing, but variation was unrelated to population size, density, pollen limitation, or autonomous selfing ability. Outcrossing rate was significantly influenced by an interaction between autonomous selfing ability and pollen limitation. Across highly autonomous populations, elevated pollen limitation was associated with reduced outcrossing, while there was no relationship for less autonomous populations. CONCLUSIONS: Both the ability to self autonomously and pollen limitation interact to shape outcrossing rates in C. americana. This work suggests that autonomy affords mating-system flexibility, though it is not ubiquitous in all populations across the species range. Interactions between traits influencing autonomy and pollen limitation are likely to explain variation in outcrossing rates among populations of flowering plants.

Effects of life history and ecology on virus evolutionary potential.

The life history traits of viruses pose many consequences for viral population structure. In turn, population structure may influence the evolutionary trajectory of a virus. Here we review factors that affect the evolutionary potential of viruses, including rates of mutation and recombination, bottlenecks, selection pressure, and ecological factors such as the requirement for hosts and vectors. Mutation, while supplying a pool of raw genetic material, also results in the generation of numerous unfit mutants. The infection of multiple host species may expand a virus' ecological niche, although it may come at a cost to genetic diversity. Vector-borne viruses often experience a diminished frequency of positive selection and exhibit little diversity, and resistance against vector-borne viruses may thus be more durable than against non-vectored viruses. Evidence indicates that adaptation to a vector is more evolutionarily difficult than adaptation to a host. Overall, a better understanding of how various factors influence viral dynamics in both plant and animal pathosystems will lead to more effective anti-viral treatments and countermeasures.

Bottlenecks and inbreeding depression in autotetraploids.

Inbreeding depression is dependent on the ploidy of populations and can inhibit the evolution of selfing. While polyploids should generally harbor less inbreeding depression than diploids at equilibrium, it has been unclear whether this pattern holds in non-equilibrium conditions following bottlenecks. We use stochastic individual-based simulations to determine the effects of population bottlenecks on inbreeding depression in diploids and autotetraploids, in addition to cases where neo-autotetraploids form from the union of unreduced gametes. With a ploidy-independent dominance function based on enzyme kinetics, inbreeding depression is generally lower in autotetraploids for fully and partially recessive mutations. Due to the sampling of more chromosomes during reproduction, bottlenecks generally reduce inbreeding depression to a lesser extent in autotetraploids. All else being equal, population bottlenecks may have ploidy-dependent effects for another reason-in some cases matings between close relatives temporarily increase inbreeding depression in autotetraploids by increasing the frequency of the heterozygous genotype harboring the most harmful mutations. When neo-autotetraploids are formed by few individuals, inbreeding depression is dramatically reduced, given extensive masking of harmful mutations following whole genome duplication. This effect persists as nascent tetraploids reach mutation-selection-drift balance, providing a transient period of permissive conditions favoring the evolution of selfing.

A geographic cline in the ability to self-fertilize is unrelated to the pollination environment.

The reproductive assurance (RA) hypothesis predicts that the ability to autonomously self-fertilize should be favored in environments where a lack of mates or pollinators limits outcross reproduction. Because such limits to outcrossing are predicted to be most severe at range edges, elevated autonomy in peripheral populations is often attributed to RA. We test this hypothesis in 24 populations spanning the range of Campanula americana, including sampling at the range interior and three geographic range edges. We scored autonomous fruit set in a pollinator-free environment and detected clinal variation-autonomy increased linearly from the southern to the northern edge, and from the eastern to the western edge. We then address whether the cline reflects the contemporary pollination environment. We measured population size, plant density, pollinator visitation, outcross pollen limitation and RA in natural populations over two years. Most populations were pollen limited, and those that experienced higher visitation rates by bumblebees had reduced pollen limitation. Reproductive assurance, however, was generally low across populations and was unrelated to pollen limitation or autonomy. Neither pollen limitation nor RA displayed geographic clines. Finally, autonomy was not associated with pollinator visitation rates or mate availability. Thus, the data do not support the RA hypothesis; clinal variation in autonomy is unrelated to the current pollination environment. Therefore, geographic patterns of autonomy are likely the result of historical processes rather than contemporary natural selection for RA.

Common garden test of range limits as predicted by a species distribution model in the annual plant Mimulus bicolor.

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.

Self-compatibility is over-represented on islands.

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.

Costs of selfing prevent the spread of a self-compatibility mutation that causes reproductive assurance.

In flowering plants, shifts from outcrossing to partial or complete self-fertilization have occurred independently thousands of times, yet the underlying adaptive processes are difficult to discern. Selfing's ability to provide reproductive assurance when pollination is uncertain is an oft-cited ecological explanation for its evolution, but this benefit may be outweighed by costs diminishing its selective advantage over outcrossing. We directly studied the fitness effects of a self-compatibility mutation that was backcrossed into a self-incompatible (SI) population of Leavenworthia alabamica, illuminating the direction and magnitude of selection on the mating-system modifier. In array experiments conducted in two years, self-compatible (SC) plants produced 17-26% more seed, but this advantage was counteracted by extensive seed discounting-the replacement of high-quality outcrossed seeds by selfed seeds. Using a simple model and simulations, we demonstrate that SC mutations with these attributes rarely spread to high frequency in natural populations, unless inbreeding depression falls below a threshold value (0.57 ≤ δthreshold ≤ 0.70) in SI populations. A combination of heavy seed discounting and inbreeding depression likely explains why outcrossing adaptations such as self-incompatibility are maintained generally, despite persistent input of selfing mutations, and frequent limits on outcross seed production in nature.

Evolution: Selfing Takes Species Down Stebbins's Blind Alley.

Shifts from outcrossing to selfing have occurred thousands of times across the tree of life. By reducing the size of the gene pool, selfing should limit adaptive potential. A refreshing empirical experiment with snails supports this long-standing hypothesis.

Diverse ecological relations of male gametophyte populations in stylar environments.

PREMISE OF STUDY: Pollen on a stigma represents a local population of male gametophytes vying for access to female gametophytes in the associated ovary. As in most populations, density-independent and density-dependent survival depend on intrinsic characteristics of male gametophytes and environmental (pistil) conditions. These characteristics and conditions could differ among flowers, plants, populations, and species, creating diverse male-gametophyte population dynamics, which can influence seed siring and production. METHODS: For nine species, we characterized the relations of both the mean and standard deviation of pollen-tube number at the style base to pollen receipt with nonlinear regression. Models represented asymptotic or peaked relations, providing information about the incidence and magnitude of facilitation and competition, the spatial and temporal characteristics of competition, and the intensity and relative timing of density-independent mortality. KEY RESULTS: We infer that pollen tubes of most species competed sequentially, their tips ceasing growth if earlier tubes had depleted stylar space/resources; although two species experienced simultaneous competition. Tube success of three species revealed positive density dependence (facilitation) at low density. For at least four species, density-independent mortality preceded competition. Tube success varied mostly within plants, rather than among plants or conspecific populations. Pollen quality influenced tube success for two of three species; affecting density-independent survival in one and density-dependent performance in the other. CONCLUSIONS: The diverse relations of pollen-tube success to pollen receipt evident among just nine species indicate significant contributions of the processes governing pollen germination and tube growth to the reproductive diversity of angiosperms.

Environmental and genetic correlates of allocation to sexual reproduction in the circumpolar plant Bistorta vivipara.

UNLABELLED: • PREMISE OF THE STUDY: Sexual reproduction often requires more energy and time than clonal reproduction. In marginal arctic conditions, species that can reproduce both sexually and clonally dominate. Plants with this capacity may thrive because they can alter reproduction depending on environmental conditions. Bistorta vivipara is a circumpolar herb that predominately reproduces clonally, but certain environmental conditions promote higher investment in flowers (and possible sexual reproduction). Despite largely reproducing clonally, the herb has high levels of genetic variation, and the processes underlying this paradoxical pattern of variation remain unclear. Here we identified environmental factors associated with sexual investment and examined whether sexual reproduction is associated with higher levels of genetic variation.• METHODS: We sampled 20 populations of B. vivipara across the high Arctic archipelago of Svalbard. In each population, we measured reproductive traits, environmental variables, and collected samples for genetic analyses. These samples permitted hypotheses to be tested regarding sexual investment and ecological and genetic correlates.• KEY RESULTS: Increased soil nitrogen and organic matter content and decreased elevation were positively associated with investment in flowers. Increased investment in flowers significantly correlated with more genotypes per population. Linkage disequilibrium was consistent with predominant clonality, but several populations showed higher genetic variation and lower differentiation than expected. There was no geographical genetic structure.• CONCLUSIONS: In B. vivipara, sexual investment is positively associated with habitat quality. Bistorta vivipara predominantly reproduces clonally, but occasional outcrossing, efficient clonal reproduction, and dispersal by bulbils can explain the considerable genetic variation and weak genetic structure in B. vivipara.

The scope of Baker's law.

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.

A General Model of Negative Frequency Dependent Selection Explains Global Patterns of Human ABO Polymorphism.

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.