Josh R. Auld

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.

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

Abstract 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 (FIS-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 FIS-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.

Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity

Phenotypic plasticity is ubiquitous and generally regarded as a key mechanism for enabling organisms to survive in the face of environmental change. Because no organism is infinitely or ideally plastic, theory suggests that there must be limits (for example, the lack of ability to produce an optimal trait) to the evolution of phenotypic plasticity, or that plasticity may have inherent significant costs. Yet numerous experimental studies have not detected widespread costs. Explicitly differentiating plasticity costs from phenotype costs, we re-evaluate fundamental questions of the limits to the evolution of plasticity and of generalists vs specialists. We advocate for the view that relaxed selection and variable selection intensities are likely more important constraints to the evolution of plasticity than the costs of plasticity. Some forms of plasticity, such as learning, may be inherently costly. In addition, we examine opportunities to offset costs of phenotypes through ontogeny, amelioration of phenotypic costs across environments, and the condition-dependent hypothesis. We propose avenues of further inquiry in the limits of plasticity using new and classic methods of ecological parameterization, phylogenetics and omics in the context of answering questions on the constraints of plasticity. Given plasticity’s key role in coping with environmental change, approaches spanning the spectrum from applied to basic will greatly enrich our understanding of the evolution of plasticity and resolve our understanding of limits.

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.

PREDATOR- AND COMPETITOR-INDUCED PLASTICITY: HOW CHANGES IN FORAGING MORPHOLOGY AFFECT PHENOTYPIC TRADE-OFFS

Studies of phenotypic plasticity frequently demonstrate functional trade-offs between alternative phenotypes by documenting environment-specific costs and benefits. However, the functional mechanisms underlying these trade-offs are often unknown. For example, predator-induced traits typically provide superior predator resistance but slower growth, while competitor-induced traits provide better growth but inferior predator resistance. While the mechanisms underlying predator resistance have been identified, the mechanisms underlying differential growth have remained elusive. To determine whether competitor and predator environments affect individual growth by induced changes in foraging morphology, we raised wood frog tadpoles (Rana sylvatica) under a factorial combination of competitors and predators and assessed changes in mouthparts that might affect growth. In general, competitors induced relatively larger oral discs, wider beaks, and longer tooth rows, while predators induced relatively smaller oral discs, narrower beaks, and shorter tooth rows. These effects were interactive; the largest competitor-induced responses occurred under high predator density and the largest predator-induced responses occurred under low competition. Further, one of the tooth rows that commonly appeared under low predation risk was frequently absent under high predation risk. These discoveries suggest that predator and competitor environments can have profound effects on prey foraging structures and that these effects set up growth trade-offs between phenotypes that favor the evolution of phenotypically plastic responses.

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.

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.

The scope of Baker's law

Bakers 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 Bakers 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 Bakers law fall away when a narrower perspective is adopted on how it should be circumscribed. We emphasize that Bakers 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 Bakers 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.

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.

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.