Effect of Predator-Prey Phylogenetic Similarity on the Fitness Consequences of Predation: A Trade-off between Nutrition and Disease?

A largely neglected aspect of foraging behavior is whether the costs and benefits of predation vary as a function of phylogenetic (i.e., genetic) similarity between predator and prey. Prey of varying phylogenetic similarities to predators might differ in value because both the risk of pathogen transmission and the nutritional quality of prey typically decline with decreasing phylogenetic similarity between predator and prey. I experimentally evaluated this hypothesis by feeding omnivorous spadefoot toad tadpoles (Spea bombifrons, Spea multiplicata, and Scaphiopus couchii) either conspecific tadpoles or an equal mass of three different species of heterospecific prey, all of which contained naturally occurring bacteria. I also examined which prey species Spea tadpoles preferred. I found that all three species of tadpoles performed best on, and preferred to eat, prey that were of intermediate phylogenetic similarity to the predators. Prey of intermediate phylogenetic similarity may provide the greatest fitness benefits to predators because such prey balance the nutritional benefits of closely related prey with the cost of parasite transmission between closely related individuals

Imperfect Mimicry and the Limits of Natural Selection

Mimicry—when one organism (the mimic) evolves a phenotypic resemblance to another (the model) due to selective benefits—is widely used to illustrate natural selection’s power to generate adaptations. However, many putative mimics resemble their models imprecisely, and such imperfect mimicry represents a specific challenge to mimicry theory and a general one to evolutionary theory. Here, we discuss 11 nonmutually exclusive hypotheses for imperfect mimicry. We group these hypotheses according to whether imperfect mimicry reflects: an artifact of human perception, which is not shared by any naturally occurring predators and therefore is not truly an instance of imperfect mimicry; genetic, developmental, or time-lag constraints, which (temporarily) prevent a response to selection for perfect mimicry; relaxed selection, where imperfect mimicry is as adaptive as perfect mimicry; or tradeoffs, where imperfect mimicry is (locally) more adaptive than perfect mimicry. We find that the relaxed selection hypothesis has garnered the most support. However, because only a few study systems have thus far been comprehensively evaluated, the relative contributions of the various hypotheses toward explaining the evolution of imperfect mimicry remain unclear. Ultimately, clarifying why imperfect mimicry exists should provide critical insights into the limits of natural selection in producing complex adaptations

Condition-dependent expression of trophic polyphenism: effects of individual size and competitive ability

Understanding the adaptive significance of alternative phenotypes may require knowing how the internal state of an organism affects the relationship between phenotypic variation and fitness across selective environments. Here, we explore how individual state interacts with environmental variation to affect expression of a trophic polyphenism in larval amphibians. Following the consumption of fairy shrimp, typical omnivorous plains spadefoot toad tadpoles (Spea bombifrons) may express an alternative 'carnivore' phenotype. The carnivore phenotype confers rapid growth and development, but these benefits come at the expense of condition at metamorphosis. Larval habitats vary in longevity, food availability and tadpole morph frequency, each of which potentially affects the relationship between tadpole state (e.g. size) and morph fitness. Hence, we predicted that phenotype expression should depend on both tadpole size and larval environment. We found that small tadpoles were more likely to develop into carnivores than large tadpoles when each was raised in isolation. When tadpoles were raised in pairs, however, relatively smaller tadpoles were less likely to express the carnivore phenotype than larger tadpoles. We present results to support the hypothesis that these contrasting effects of absolute and relative size on carnivore morph expression stem from the effects of tadpole size on the ability to consume fairy shrimp. We conclude that competition for shrimp imposed by larger tadpoles may often inhibit relatively smaller tadpoles from expressing the carnivore phenotype. Thus, we find support for our prediction that morph expression in Spea depends on both an individual's internal state and larval environment. Our understanding of the adaptive significance and, ultimately, the evolution of this and other state-dependent responses may be enhanced by considering how interactions among individuals affect the relationships among fitness, internal state and phenotype expression across different selective environments

A TEST OF ALTERNATIVE HYPOTHESES FOR CHARACTER DIVERGENCE BETWEEN COEXISTING SPECIES

Why do closely related, coexisting species typically differ in phenotypic features associated with resource use? One answer to this question is that such differences might generally evolve in allopatry, as different species adapt to divergent environmental conditions, and any differences that thereby accumulate might subsequently enable coexistence in sympatry. Alternatively, coexisting species might generally diverge in sympatry, because of selection to reduce competition for food (character displacement). Here we evaluated these two causes of character divergence by asking which hypothesis better explains differences in feeding morphology between tadpoles of two species of spadefoot toads, Spea bombifrons and S. multiplicata. We found that, in natural ponds containing both species, S. multiplicata almost always developed into a smaller, round-bodied tadpole with normal sized jaw muscles used for feeding on detritus at the pond bottom (the omnivore morph), whereas S. bombifrons almost always developed into a larger, flat-headed tadpole with greatly enlarged jaw muscles used for feeding on crustaceans in open water (the carnivore morph). By contrast, in all but one of 18 similar ponds containing a single species, both species expressed both phenotypes. Divergence between species in morph production appears to have evolved in sympatry: when we compared population means for each of four key trophic characters, we found that no allopatric population of S. bombifrons was as carnivore-like as the sympatric S. bombifrons, and, for three of four characters, no allopatric population of S. multiplicata was as omnivore-like as the sympatric S. multiplicata. In contrast to significant differences in trophic characters, we found no divergence between allopatric and sympatric populations in a character not directly involved in feeding on detritus or crustaceans (overall body size). These data, together with our earlier experimental work, reveal that coexisting S. bombifrons and S. multiplicata have diverged from one another in resource use and in phenotypic features associated with resource use because of selection to reduce competition for food (i.e., character displacement). Spea tadpoles, therefore, are one of few systems for which both experimental and observational evidence link phenotypic divergence to resource competition, thereby providing a model for understanding why coexisting species often differ phenotypically

Genetic assimilation: a review of its potential proximate causes and evolutionary consequences

Background Most, if not all, organisms possess the ability to alter their phenotype in direct response to changes in their environment, a phenomenon known as phenotypic plasticity. Selection can break this environmental sensitivity, however, and cause a formerly environmentally induced trait to evolve to become fixed through a process called genetic assimilation. Essentially, genetic assimilation can be viewed as the evolution of environmental robustness in what was formerly an environmentally sensitive trait. Because genetic assimilation has long been suggested to play a key role in the origins of phenotypic novelty and possibly even new species, identifying and characterizing the proximate mechanisms that underlie genetic assimilation may advance our basic understanding of how novel traits and species evolve

Evaluating ‘Plasticity-First’ Evolution in Nature: Key Criteria and Empirical Approaches

Many biologists are asking whether environmentally initiated phenotypic change (i.e., 'phenotypic plasticity') precedes, and even facilitates, evolutionary adaptation. However, this 'plasticity-first' hypothesis remains controversial, primarily because comprehensive tests from natural populations are generally lacking. We briefly describe the plasticity-first hypothesis and present much-needed key criteria to allow tests in diverse, natural systems. Furthermore, we offer a framework for how these criteria can be evaluated and discuss examples where the plasticity-first hypothesis has been investigated in natural populations. Our goal is to provide a means by which the role of plasticity in adaptive evolution can be assessed

Character Displacement: Ecological And Reproductive Responses To A Common Evolutionary Problem

Character displacement – trait evolution stemming from selection to lessen resource competition or reproductive interactions between species – has long been viewed as an important mechanism for enabling closely related species to coexist. Yet, the causes and consequences of character displacement have not been fully explored. Moreover, character displacement in traits associated with resource use (ecological character displacement) has been studied largely independently of that in traits associated with reproduction (reproductive character displacement). Here, we underscore the commonalities of these two forms of character displacement and discuss how they interact. We focus on the causes of character displacement and explore how character displacement can have downstream effects ranging from speciation to extinction. In short, understanding how organisms respond to competitive and reproductive interactions with heterospecifics offers key insights into the evolutionary consequences of species coexistence and diversification

Development and Evolution of Character Displacement

Character displacement occurs when competition for either resources or successful reproduction imposes divergent selection on interacting species, causing divergence in traits associated with resource use or reproduction. Here, we describe how character displacement can be mediated either by genetically canalized changes (i.e., changes that reflect allelic or genotype frequency changes) or by phenotypic plasticity. We also discuss how these two mechanisms influence the tempo of character displacement. Specifically, we suggest that, under some conditions, character displacement mediated by phenotypic plasticity might occur more rapidly than that mediated by genetically canalized changes. Finally, we describe how these two mechanisms may act together and determine character displacement’s mode, such that it proceeds through an initial phase in which trait divergence is environmentally induced to a later phase in which divergence becomes genetically canalized. This plasticity-first hypothesis predicts that character displacement should be generally mediated by ancestral plasticity and that it will arise similarly in multiple, independently evolving populations. We conclude by highlighting future directions for research that would test these predictions

Character Displacement and the Origins of Diversity

In The Origin of Species, Darwin proposed his ‘principle of divergence of character’ (a process now termed ‘character displacement’) to explain how new species arise and why they differ from one other phenotypically. Darwin maintained that the origin of species, and the evolution of differences between them, is ultimately caused by divergent selection acting to minimize competitive interactions between initially similar individuals, populations, and species. Here, we examine the empirical support for the various claims that constitute Darwin’s principle, specifically that: (1) competition promotes divergent trait evolution; (2) the strength of competitively mediated divergent selection increases with increasing phenotypic similarity between competitors; (3) divergence can occur within species; and (4) competitively mediated divergence can trigger speciation. We also explore aspects that Darwin failed to consider. In particular, we describe how: (1) divergence can arise from selection acting to lessen reproductive interactions; (2) divergence is fueled by the intersection of character displacement and sexual selection; and (3) phenotypic plasticity may play a key role in promoting character displacement. Generally, character displacement is well supported empirically, and it remains a vital explanation for how new species arise and diversify

A Batesian mimic and its model share color production mechanisms

Batesian mimics are harmless prey species that resemble dangerous ones (models), and thus receive protection from predators. How such adaptive resemblances evolve is a classical problem in evolutionary biology. Mimicry is typically thought to be difficult to evolve, especially if the model and mimic produce the convergent phenotype through different proximate mechanisms. However, mimicry may evolve more readily if mimic and model share similar pathways for producing the convergent phenotype. In such cases, these pathways can be co-opted in ancestral mimic populations to produce high-fidelity mimicry without the need for major evolutionary innovations. Here, we show that a Batesian mimic, the scarlet kingsnake Lampropeltis elapsoides, produces its coloration using the same physiological mechanisms as does its model, the eastern coral snake Micrurus fulvius. Therefore, precise color mimicry may have been able to evolve easily in this system. Generally, we know relatively little about the proximate mechanisms underlying mimicry