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Hermaphroditic individuals can produce both selfed and outcrossed progeny, termed mixed mating. General theory predicts that mixed-mating populations should evolve quickly toward high rates of setting, driven by rapid purging of genetic load and loss of inbreeding depression (ID), but the substantial number of mixed-mating species observed in nature calls this prediction into question. Lower average ID reported for selfing than for outcrossing populations is consistent with purging and suggests that mixed-mating taxa in evolutionary transition will have intermediate ID. We compared the magnitude of ID from published estimates for highly selfing (r > 0.8), mixed-mating (0.2 ≤ r ≥ 0.8), and highly outcrossing (r < 0.2) plant populations across 58 species. We found that mixed-mating and outcrossing taxa have equally high average lifetime ID (δ = 0.58 and 0.54, respectively) and similar ID at each of four life-cycle stages. These results are not consistent with evolution toward selfing in most mixed-mating taxa. We suggest that prevention of purging by selective interference could explain stable mixed mating in many natural populations. We identify critical gaps in the empirical data on ID and outline key approaches to filling them.

Male–female coevolution has taken different paths among closely related species, but our understanding of the factors that govern its direction is limited. While it is clear that ecological factors, life history, and the economics of reproduction are connected, the divergent links are often obscure. We propose that a complete understanding requires the conceptual integration of metabolic phenotypes. Metabolic rate, a nexus of life history evolution, is constrained by ecological factors and may exert important direct and indirect effects on the evolution of sexual dimorphism. We performed standardized experiments in 12 seed beetle species to gain a rich set of sex-specific measures of metabolic phenotypes, life history traits, and the economics of mating and analyzed our multivariate data using phylogenetic comparative methods. Resting metabolic rate (RMR) showed extensive evolution and evolved more rapidly in males than in females. The evolution of RMR was tightly coupled with a suite of life history traits, describing a pace-of-life syndrome (POLS), with indirect effects on the economics of mating. As predicted, high resource competition was associated with a low RMR and a slow POLS. The cost of mating showed sexually antagonistic coevolution, a hallmark of sexual conflict. The sex-specific costs and benefits of mating were predictably related to ecology, primarily through the evolution of male ejaculate size. Overall, our results support the tenet that resource competition affects metabolic processes that, in turn, have predictable effects on both life history evolution and reproduction, such that ecology shows both direct and indirect effects on male–female coevolution.

Premise of Study In a seminal body of theory, Lloyd showed that the fitness consequences of selfing will depend on its timing in anthesis. Selfing that occurs after opportunities for outcrossing or pollen dispersal can provide reproductive assurance when pollinators are limited and is expected to incur little cost, even when inbreeding depression is high. As a result, delayed selfing is often interpreted as a “best‐of‐both‐worlds” mating system that combines the advantages of selfing and outcrossing. Methods We surveyed 65 empirical studies of delayed selfing, recording floral mechanisms and examining information on inbreeding depression, autofertility, and other parameters to test the support for delayed selfing as a best‐of‐both‐worlds strategy. Key Results Phylogenetic distribution of the diverse floral mechanisms suggests that some basic floral structures may predispose plant taxa to evolve delayed selfing. Delayed selfing appears to serve as a best‐of‐both‐worlds strategy in some but not all species. While the capacity for autonomous selfing is often high, it is lower, in some cases, than in related species with earlier modes of selfing. In other delayed‐selfers, low inbreeding depression and reduced investment in corollas and pollen suggest limited benefits from outcrossing. Conclusions Despite a growing literature on the subject, experimental evidence for delayed selfing is limited and major gaps in knowledge remain, particularly with respect to the stability of delayed selfing and the conditions that may favor transitions between delayed and earlier selfing. Finally, we suggest a potential role of delayed selfing in facilitating transitions from self‐incompatibility to selfing.

Plant mating systems play a key role in structuring genetic variation both within and between species. In hybrid zones, the outcomes and dynamics of hybridization are usually interpreted as the balance between gene flow and selection against hybrids. Yet, mating systems can introduce selective forces that alter these expectations; with diverse outcomes for the level and direction of gene flow depending on variation in outcrossing and whether the mating systems of the species pair are the same or divergent. We present a survey of hybridization in 133 species pairs from 41 plant families and examine how patterns of hybridization vary with mating system. We examine if hybrid zone mode, level of gene flow, asymmetries in gene flow and the frequency of reproductive isolating barriers vary in relation to mating system/s of the species pair. We combine these results with a simulation model and examples from the literature to address two general themes: (1) the two-way interaction between introgression and the evolution of reproductive systems, and (2) how mating system can facilitate or restrict interspecific gene flow. We conclude that examining mating system with hybridization provides unique opportunities to understand divergence and the processes underlying reproductive isolation.

In most mammals, both sexes display different survial patterns, often involving faster senescence in males. Being under intense sexual competition to secure mating opportunities, males of polygynous species allocate resources to costly behaviors and conspicuous sexual traits, which might explain these observed differences in longevity and senescence patterns. However, comparative studies performed to date have led to conflicting results. We aimed to resolve this problem by first reviewing case studies of the relationship between the strength of sexual selection and age-specific survival metrics. Then, we performed a comprehensive comparative analysis to test whether such relationships exist among species of captive ruminants. We found that the strength of sexual selection negatively influenced the onset of actuarial senescence in males, with males senescing earlier in polygynous than in monogamous species, which led to reduced male longevity in polygynous species. Moreover, males of territorial species senesced earlier but slower, and have a shorter longevity than males of species displaying other mating tactics. We detected little influence of the strength of sexual selection on the rate of actuarial senescence. Our findings demonstrate that the onset of actuarial senescence, rather than its rate, is a side effect of physiological mechanisms linked to sexual selection, and potentially accounts for observed differences in longevity.

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.

Reduced allocation to structures for pollinator attraction is predicted in selfing species. We explored the association between outcrossing and floral display in a broad sample of angiosperms. We used the demonstrated relationship to test for bias against selfing species in the outcrossing rate distribution, the shape of which has relevance for the stability of mixed mating. Relationships between outcrossing rate, flower size, flower number and floral display, measured as the product of flower size and number, were examined using phylogenetically independent contrasts. The distribution of floral displays among species in the outcrossing rate database was compared with that of a random sample of the same flora. The outcrossing rate was positively associated with the product of flower size and number; individually, components of display were less strongly related to outcrossing. Compared with a random sample, species in the outcrossing rate database showed a deficit of small floral display sizes. We found broad support for reduced allocation to attraction in selfing species. We suggest that covariation between mating systems and total allocation to attraction can explain the deviation from expected trade-offs between flower size and number. Our results suggest a bias against estimating outcrossing rates in the lower half of the distribution, but not specifically against highly selfing species.

In polygynandrous mating systems, the factors that mediate copulation success and the use of alternative mating tactics, such as mate guarding, are still poorly understood. In the rock hyrax (Procavia capensis), both sexes mate annually with multiple partners during a single month. In order to examine the factors that drive copulation success, we used 494 mating-related observations that were collected over a decade. In our analysis, we used the traits of individual hyraxes as well as the traits of members of their sexual niche, which we defined as their local competitors and potential mates. Using individual traits, we found that overall, female hyraxes rejected copulation attempts more frequently than males, supporting predictions from sexual selection theory. Females who had been mothers in previous years were mate-guarded more by resident males. When we considered the traits of competitors and potential mates in individuals’ sexual niche, we found that when resident males had higher-ranking competitors, their copulation success decreased, irrespective of their own traits. Bachelor male copulation success was not influenced by their competitor’s social status. Female copulation success was positively affected by maternal status and by social network position. Females that were central in the social network and those that had central female competitors had higher copulation success, supporting the benefits of social cohesion and the importance of the social niche. Thus, our results suggest that in polygynandrous mating systems, copulation success is determined not only by individual quality but also by the social and sexual niches that the individual occupies. SIGNIFICANCE STATEMENT: Social networks describe with whom individuals consort. The complex patterns of sexual relationships in animal societies can also be expressed as networks of mating-related interactions. During our long-term study on the dynamic social relationships of wild rock hyraxes, we observed complex sexual interactions. Our results show that hyraxes choose mating partners from their available mate pool (or sexual niche) taking into account the traits of their actual mates, other potential mates, and those of their competitors. These findings suggest that the sexual niche, describing the subset of available mating partners, is important for mate choice, with significant implications to the study of sexual selection.

Mixed mating and variation in outcrossing rate among populations of the same species are common. Outcrossing can be affected by pollinator activity and floral traits that facilitate or impede autonomous self‐fertilization. However, the relative contribution of pollen limitation and evolved differences in the ability to self‐fertilize to variation in the mating system is poorly understood and can only be disentangled using an experimental approach. We placed arrays of plants from eight Campanula americana populations that varied in autonomous selfing ability (hereafter “autonomy”) in sun and shade habitats to create high‐ and low‐pollination environments. Floral visitors were observed and pollen limitation, dichogamy, herkogamy and pollen persistence within the flower were measured. Outcrossing rate was estimated for a subset of the arrays. Pollen limitation was over three times higher in the shade than the sun due to differences in pollinator visitation. Populations with high levels of autonomy displayed greater pollen persistence and dichogamy in the more pollen‐limited environments than in the high‐pollination environments. In these high‐autonomy populations, outcrossing rates were tightly associated with pollen limitation, with reduced outcrossing under strong pollen limitation. In contrast, populations with intermediate autonomy levels had less plastic floral traits and their outcrossing rates changed little with pollen limitation. Mating system was shaped by both the pollination environment and the magnitude of plasticity in floral traits. The experimental approach used here revealed that plasticity in floral traits provides the ability to adjust mating system in response to limited potential for outcrossing. The lack of plasticity in some populations could explain mismatches between pollinator activity and mating system in natural populations. Finally, flexibility in the mating system may help explain the prevalence of mixed mating. A plain language summary is available for this article. Plain Language Summary

A crucial step in the transition from outcrossing to self-fertilization is the loss of genetic self-incompatibility (SI). In the Brassicaceae, SI involves the interaction of female and male specificity components, encoded by the genes SRK and SCR at the self-incompatibility locus (S-locus). Theory predicts that S-linked mutations, and especially dominant mutations in SCR, are likely to contribute to loss of SI. However, few studies have investigated the contribution of dominant mutations to loss of SI in wild plant species. Here, we investigate the genetic basis of loss of SI in the self-fertilizing crucifer species Capsella orientalis, by combining genetic mapping, long-read sequencing of complete S-haplotypes, gene expression analyses and controlled crosses. We show that loss of SI in C. orientalis occurred < 2.6 Mya and maps as a dominant trait to the S-locus. We identify a fixed frameshift deletion in the male specificity gene SCR and confirm loss of male SI specificity. We further identify an S-linked small RNA that is predicted to cause dominance of self-compatibility. Our results agree with predictions on the contribution of dominant S-linked mutations to loss of SI, and thus provide new insights into the molecular basis of mating system transitions.