Optimal Mating Strategies for Preferentially Outcrossing Simultaneous Hermaphrodites in the Presence of Predators.

The optimal timing for initiating reproduction (i.e., the age at first reproduction) is a critical life history trait describing aspects of an individual's resource-allocation strategy. Recent theoretical and empirical work has demonstrated that this trait is also tied to mating system expression when individuals have the opportunity to reproduce via both self-fertilization and cross-fertilization. A strategy of "delayed selfing" has emerged as a "best of both worlds" arrangement where, in the absence of a mate, an individual will delay reproduction (selfing) to "wait" for a mate. Herein, we extend previously developed predictive optimization models for the timing of reproduction to a situation where organisms can allocate their resources to size-dependent and size-independent defensive strategies to counter the threat of predation. By incorporating inducible defenses into a predictive framework for analyzing life history expression and evolution, we can more accurately evaluate the role that allocation strategy plays in altering the optimal waiting time. We compare our model to previous models and empirical results highlighting that incorporation of inducible defenses into the model broadens the parameter space in which a waiting time is expected and often leads to a predicted waiting time that is longer than in the situation without inducible defenses. In particular, a waiting time is predicted to exist regardless of the strength of inbreeding depression in the population.

The effects of diet and mating system on reproductive (and post-reproductive) life span in a freshwater snail.

The length of the reproductive life span, along with the number/frequency/magnitude of reproductive events, quantifies an individual's potential contribution to the next generation. By examining reproductive life span, and distinguishing it from somatic life span, we gain insight into critical aspects of an individual's potential fitness as well as reproductive and somatic senescence. Additionally, differentiating somatic and reproductive life spans can provide insight into the existence of a post-reproductive period and factors that shape its duration. Given the known importance of diet and mating system on resource allocation, I reared individual freshwater snails (Physa acuta) from 22 full-sib families under a 2 × 2 factorial design that crossed mate availability (available [outcrossing] or not [selfing]) and diet (Spirulina or lettuce) and quantified aspects of the entire life history enabling me to distinguish reproductive and somatic life spans, determine the total number of reproductive events, and evaluate how the reproductive rate changes with age. Overall, mated snails experienced shorter reproductive and somatic life spans; a diet of Spirulina also shortened both reproductive and somatic life spans. A post-reproductive period existed in all conditions; its duration was proportional to somatic but not reproductive life span. I evaluate several hypotheses for the existence and duration of the post-reproductive period, including a novel hypothesis that the post-reproductive period may result from an increase in reproductive interval with age. I conclude that the post-reproductive period may be indicative of a randomly timed death occurring as the interval between reproductive events continues to increase. As such, a "post-reproductive" period can be viewed as a by-product of a situation where reproductive senescence outpaces somatic senescence.

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.

Age-dependent effects of predation risk on reproductive success in a freshwater snail.

Reproductive performance is often age-dependent, showing patterns of improvement and/or senescence as well as trade-offs with other traits throughout the lifespan. High levels of extrinsic mortality (e.g., from predators) have been shown to sometimes, but not always, select for accelerated actuarial senescence in nature and in the lab. Here, we explore the inductive (i.e., plastic) effects of predation risk (i.e., nonlethal exposure to chemical cues from predators) on the reproductive success of freshwater snails (Physa acuta). Snails were reared either in the presence or absence of chemical cues from predatory crayfish and mated early in life or late in life (a 2 × 2 factorial design); we measured egg hatching and early post-hatching survival of their offspring. Both age and predation risk reduced reproductive success, illustrating that predation risk can have a cross-generational effect on the early survival of juveniles. Further, the decline in reproductive success was over three times faster under predation risk compared to the no-predator treatment, an effect that stemmed from a disproportionate, negative effect of predation risk on the post-hatching survival instead of hatching rate. We discuss our results in terms of a hypothesized consequence of elevated stress hormone levels.

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.

Diet alters delayed selfing, inbreeding depression, and reproductive senescence in a freshwater snail.

Reproductive success is a critical fitness attribute that is directly influenced by resource availability. Here, we investigate the effects of diet-based resource availability on three interrelated aspects of reproductive success: a change in mating system based on mate availability, consequent inbreeding depression, and the deterioration of reproductive efficiency with age (senescence). We employed a factorial experimental design using 22 full-sib families of the hermaphroditic freshwater snail Physa acuta to explore these interactions. Individual snails were reared in one of two mate-availability treatments (isolated [selfing] or occasionally paired [outcrossing]) and one of two diet treatments (boiled lettuce or Spirulina, an algae that is rich in protein, vitamins, and minerals). Spirulina-fed snails initiated reproduction at a 13% earlier age and 7% larger size than lettuce-fed snails. Spirulina also resulted in a 30% reduction in the time delay before selfing. Compared to lettuce, a diet of Spirulina increased inbreeding depression by 52% for egg hatching rate and 64% for posthatching juvenile survival. Furthermore, Spirulina led to a 15-fold increase in the rate of reproductive senescence compared with a diet of lettuce. These transgenerational, interactive effects of diet on inbreeding depression and reproductive senescence are discussed in the context of diet-induced phenotypic plasticity.

Does energy availability predict gastropod reproductive strategies?

The diversity of reproductive strategies in nature is shaped by a plethora of factors including energy availability. For example, both low temperatures and limited food availability could increase larval exposure to predation by slowing development, selecting against pelagic and/or feeding larvae. The frequency of hermaphroditism could increase under low food availability as population density (and hence mate availability) decreases. We examine the relationship between reproductive/life-history traits and energy availability for 189 marine gastropod families. Only larval type was related to energy availability with the odds of having planktotrophic larvae versus direct development decreasing by 1% with every one-unit increase in the square root of carbon flux. Simultaneous hermaphroditism also potentially increases with carbon flux, but this effect disappears when accounting for evolutionary relationships among taxa. Our findings are in contrast to some theory and empirical work demonstrating that hermaphroditism should increase and planktotrophic development should decrease with decreasing productivity. Instead, they suggest that some reproductive strategies are too energetically expensive at low food availabilities, or arise only when energy is available, and others serve to capitalize on opportunities for aggregation or increased energy availability.

The evolution of seed dormancy: environmental cues, evolutionary hubs, and diversification of the seed plants.

Seed dormancy, by controlling the timing of germination, can strongly affect plant survival. The kind of seed dormancy, therefore, can influence both population and species-level processes such as colonization, adaptation, speciation, and extinction. We used a dataset comprising over 14,000 taxa in 318 families across the seed plants to test hypotheses on the evolution of different kinds of seed dormancy and their association with lineage diversification. We found morphophysiological dormancy to be the most likely ancestral state of seed plants, suggesting that physiologically regulated dormancy in response to environmental cues was present at the origin of seed plants. Additionally, we found that physiological dormancy (PD), once disassociated from morphological dormancy, acted as an 'evolutionary hub' from which other dormancy classes evolved, and that it was associated with higher rates of lineage diversification via higher speciation rates. The environmental sensitivity provided by dormancy in general, and by PD in particular, appears to be a key trait in the diversification of seed plants.

Evolutionary change in continuous reaction norms.

Understanding the evolution of reaction norms remains a major challenge in ecology and evolution. Investigating evolutionary divergence in reaction norm shapes between populations and closely related species is one approach to providing insights. Here we use a meta-analytic approach to compare divergence in reaction norms of closely related species or populations of animals and plants across types of traits and environments. We quantified mean-standardized differences in overall trait means (Offset) and reaction norm shape (including both Slope and Curvature). These analyses revealed that differences in shape (Slope and Curvature together) were generally greater than differences in Offset. Additionally, differences in Curvature were generally greater than differences in Slope. The type of taxon contrast (species vs. population), trait, organism, and the type and novelty of environments all contributed to the best-fitting models, especially for Offset, Curvature, and the total differences (Total) between reaction norms. Congeneric species had greater differences in reaction norms than populations, and novel environmental conditions increased the differences in reaction norms between populations or species. These results show that evolutionary divergence of curvature is common and should be considered an important aspect of plasticity, together with slope. Biological details about traits and environments, including cryptic variation expressed in novel environmental conditions, may be critical to understanding how reaction norms evolve in novel and rapidly changing environments.

Who wears the pants in a mute swan pair? Deciphering the effects of male and female age and identity on breeding success.

Traditionally, many breeding traits (e.g. the timing and size of clutches) were considered to be female-only traits in that males played little-to-no role in their expression. Although the contribution of males to such breeding traits, as well as other aspects of reproduction, is increasingly recognized, few studies have demonstrated the effects of male age and life history on breeding traits and, importantly, whether these effects are underlined by additive-genetic variation. Here, we take advantage of a long-term data set on mute swans (Cygnus olor) to demonstrate that the ages of both the male and female parents play significant roles in the timing and size of clutches, although recruitment success did not show similar effects. Individual males varied significantly in their influence on the timing of egg laying. We decomposed this variation using an 'animal model'; competing models that were the source of this variation as additive-genetic or permanent-environmental variation was not statistically distinguishable. Our results add to the growing evidence that reproductive performance should be considered as a product of the identity and condition of both parents.

Patterns of mating-system evolution in hermaphroditic animals: correlations among selfing rate, inbreeding depression, and the timing of reproduction.

In hermaphrodites, traits that influence the selfing rate can coevolve with inbreeding depression, leading to the emergence of evolutionary syndromes. Theory predicts a negative correlation between inbreeding depression and selfing rate across species. This prediction has only been examined and validated in vascular plants. Furthermore, selfing rates are often influenced by environmental conditions (e.g., lack of mates or pollinators), and species are predicted to evolve mechanisms to buffer this variation. We extend previous studies of mating-system syndromes in two ways. First, we assembled a new dataset on Basommatophoran snails (17 species, including new data on 12 species). Second, we measured how species responded to variation in mate availability. Specifically, we quantified the waiting time before selfing (i.e., how long the onset of reproduction is delayed in the absence of mates). Selfing rates were negatively correlated with both inbreeding depression and the waiting time. Species with stronger inbreeding depression exhibited longer waiting times. These patterns obtained on Basommatophorans still hold when including eight other hermaphroditic animals. Our results support the hypothesis that selection drives the evolution of mating-system syndromes in animals. The reaction norm of selfing rates to mate availability is a key target of natural selection in this context.

The effects of predation risk on mating system expression in a freshwater snail.

Environmental effects on mating system expression are central to understanding mating system evolution in nature. Here, I report the results from a quantitative-genetic experiment aimed at understanding the role of predation risk in the expression and evolution of life-history and mating-system traits in a hermaphroditic freshwater snail (Physa acuta). I reared 30 full-sib families in four environments that factorially contrast predation risk and mate availability and measured age/size at first reproduction, growth rate, a morphological defense, and the early survival of outcrossed/selfed eggs that were laid under predator/no-predator conditions. I evaluated the genetic basis of trade-offs among traits and the stability of the G matrix across environments. Mating reduced growth while predation risk increased growth, but the effects of mating were weaker for predator-induced snails and the effects of predation risk were weaker for snails without mates. Predation risk reduced the amount of time that individuals waited before self-fertilizing and reduced inbreeding depression in the offspring. There was a positive among-family relationship between the amount of time that individuals delayed selfing under predation risk and the magnitude of inbreeding depression. These results highlight several potential roles of enemies in mating-system expression and evolution.

Bateman gradients in hermaphrodites: an extended approach to quantify sexual selection.

Sexual selection is often quantified using Bateman gradients, which represent sex-specific regression slopes of reproductive success on mating success and thus describe the expected fitness returns from mating more often. Although the analytical framework for Bateman gradients aimed at covering all sexual systems, empirical studies are biased toward separate-sex organisms, probably because important characteristics of other systems remain incompletely treated. Our synthesis complements the existing Bateman gradient approach with three essential reproductive features of simultaneous hermaphrodites. First, mating in one sex may affect fitness via the opposite sex, for example, through energetic trade-offs. We integrate cross-sex selection effects and show how they help characterizing sexually mutualistic versus antagonistic selection. Second, male and female mating successes may be correlated, complicating the interpretation of Bateman gradients. We show how to quantify the impact of this correlation on sexual selection and propose a principal component analysis on male and female mating success to facilitate interpretation. Third, self-fertilization is accounted for by adding selfed progeny as a separate category of reproductive success to analyses of Bateman gradients. Finally, using a worked example from the snail Biomphalaria glabrata, we illustrate how the extended analytical framework can enhance our understanding of sexual selection in hermaphroditic animals and plants.

Inbreeding depression in adaptive plasticity under predation risk in a freshwater snail.

While much attention has been paid to the effects of inbreeding on fitness, this has mostly come from a genetic perspective. Consequently, the interaction between inbreeding and the environment is less well understood. To understand the effects of inbreeding in natural populations where environmental conditions are variable, we need to examine not only how the effects of inbreeding change among environments but also how inbreeding may affect the ability to respond to environmental conditions (i.e. phenotypic plasticity). We reared selfed and outcrossed hermaphroditic snails (Physa acuta) in the presence and absence of chemical cues from predatory crayfish and quantified expression of an inducible defence, an adaptively plastic response to predation risk. Overall, inbred snails exhibited reduced defences, but more importantly, inbreeding reduced the expression of predator-induced adaptive plasticity. Inbreeding depression in defensive morphology was 26 per cent and inbreeding depression in the plasticity of this trait was 48 per cent. Inbreeding depression in adaptive plasticity may be important to understanding the effects of inbreeding in nature.

Re-evaluating the costs and limits of adaptive phenotypic plasticity.

When the optimal phenotype differs among environments, adaptive phenotypic plasticity can evolve unless constraints impede such evolution. Costs and limits of plasticity have been proposed as important constraints on the evolution of plasticity, yet confusion exists over their distinction. We attempt to clarify these concepts by reviewing their categorization and measurement, highlighting how costs and limits are defined in different currencies (and may describe the same phenomenon). Conclusions from studies that measure the costs of plasticity have been equivocal, but we caution that these conclusions may be premature owing to a potentially common correlation between environment-specific trait values and the magnitude of trait plasticities (i.e. multi-collinearity) that results in imprecise and/or biased estimates of the costs. Meanwhile, our understanding of the limits of plasticity, and how they may be underlain by the costs of plasticity, is still in its infancy. Based on our re-evaluation of these constraints, we discuss areas for future research.

The role of natural enemies in the expression and evolution of mixed mating in hermaphroditic plants and animals.

Although a large portion of plant and animal species exhibit intermediate levels of outcrossing, the factors that maintain this wealth of variation are not well understood. Natural enemies are one relatively understudied ecological factor that may influence the evolutionary stability of mixed mating. In this paper, we aim for a conceptual unification of the role of enemies in mating system expression and evolution in both hermaphroditic animals and plants. We review current theory and detail the potential effects of enemies on fundamental mating system parameters. In doing so, we identify situations in which consideration of enemies alters expectations about the stability of mixed mating. Generally, we find that inclusion of the enemy dimension may broaden conditions in which mixed mating systems are evolutionarily stable. Finally, we highlight avenues ripe for future theoretical and empirical work that will advance our understanding of enemies in the expression and evolution of mixed mating in their hosts/victims, including examination of feedback cycles between victims and enemies and quantification of mating system-related parameters in victim populations in the presence and absence of enemies.

Animals mix it up too: the distribution of self-fertilization among hermaphroditic animals.

Excluding insects, hermaphroditism occurs in about one-third of animal species, providing numerous opportunities for the evolution of selfing. Here we provide an overview of reproductive traits in hermaphroditic animal species, review the distribution of selfing rates in animals, and test for ecological correlates of selfing. Our dataset (1342 selfing-rate estimates for 142 species) is 97% based on estimates derived from the analysis of population structure (F(IS)-estimates) using genetic markers. The distribution of selfing is slightly U-shaped and differs significantly from the more strongly U-shaped plant distribution with 47% of animal t-estimates being intermediate (falling between 0.2 and 0.8) compared to 42% for plants. The influence of several factors on the distribution of selfing rates was explored (e.g., number of populations studied per species, habitat, coloniality, sessility, or fertilization type), none of which significantly affect the distribution. Our results suggest that genetic forces might contribute to the evolution of self-fertilization to the same extent in animals and plants, although the high proportion of intermediate outcrossing suggests a significant role of ecological factors (e.g., reproductive assurance) in animals. However, we caution that the distribution of selfing rates in animals is affected by various factors that might bias F(IS)-estimates, including phylogenetic underrepresentation of highly selfing and outcrossing species, various genotyping errors (e.g., null alleles) and inbreeding depression. This highlights the necessity of obtaining better estimates of selfing for hermaphroditic animals, such as genotyping progeny arrays, as in plants.

Putting prey back together again: integrating predator-induced behavior, morphology, and life history.

The last decade has seen an explosion in the number of studies exploring predator-induced plasticity. Recently, there has been a call for more comprehensive approaches that can identify functional relationships between traits, constraints on phenotypic responses, and the cost and benefits of alternative phenotypes. In this study, we exposed Helisoma trivolvis, a freshwater snail, to a factorial combination of three resource levels and five predator environments (no predator, one or two water bugs, and one or two crayfish) and examined ten traits including behavior, morphology, and life history. Each predator induced a unique suite of behavioral and morphological responses. Snails increased near-surface habitat use with crayfish but not with water bugs. Further, crayfish induced narrow and high shells whereas water bugs induced wide shells and wide apertures. In terms of life history, both predators induced delayed reproduction and greater mass at reproduction. However, crayfish induced a greater delay in reproduction that resulted in reduced fecundity whereas water bugs did not induce differences in fecundity. Resource levels impacted the morphology of H. trivolvis; snails reared with greater resource levels produced higher shells, narrower shells, and wider apertures. Resource levels also impacted snail life history; lower resources caused longer times to reproduction and reduced fecundity. Based on an analysis of phenotypic correlations, the morphological responses to each predator most likely represent phenotypic trade-offs. Snails could either produce invasion-resistant shells for defense against water bugs or crush-resistant shells for defense against crayfish, but not both. Our use of a comprehensive approach to examine the responses of H. trivolvis has provided important information regarding the complexity of phenotypic responses to different environments, the patterns of phenotypic integration across environments, and the potential costs and benefits associated with plastic traits.