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

Maternal Investment Influences Expression of Resource Polymorphism in Amphibians: Implications for the Evolution of Novel Resource-Use Phenotypes

Maternal effects—where an individual's phenotype is influenced by the phenotype or environment of its mother—are taxonomically and ecologically widespread. Yet, their role in the origin of novel, complex traits remains unclear. Here we investigate the role of maternal effects in influencing the induction of a novel resource-use phenotype. Spadefoot toad tadpoles, Spea multiplicata, often deviate from their normal development and produce a morphologically distinctive carnivore-morph phenotype, which specializes on anostracan fairy shrimp. We evaluated whether maternal investment influences expression of this novel phenotype. We found that larger females invested in larger eggs, which, in turn, produced larger tadpoles. Such larger tadpoles are better able to capture the shrimp that induce carnivores. By influencing the expression of novel resource-use phenotypes, maternal effects may play a largely underappreciated role in the origins of novelty

Why Do Species Co-Occur? A Test of Alternative Hypotheses Describing Abiotic Differences in Sympatry versus Allopatry Using Spadefoot Toads

Areas of co-occurrence between two species (sympatry) are often thought to arise in regions where abiotic conditions are conducive to both species and are therefore intermediate between regions where either species occurs alone (allopatry). Depending on historical factors or interactions between species, however, sympatry might not differ from allopatry, or, alternatively, sympatry might actually be more extreme in abiotic conditions relative to allopatry. Here, we evaluate these three hypothesized patterns for how sympatry compares to allopatry in abiotic conditions. We use two species of congeneric spadefoot toads, Spea multiplicata and S. bombifrons, as our study system. To test these hypotheses, we created ecological niche models (specifically using Maxent) for both species to create a map of the joint probability of occurrence of both species. Using the results of these models, we identified three types of locations: two where either species was predicted to occur alone (i.e., allopatry for S. multiplicata and allopatry for S. bombifrons) and one where both species were predicted to co-occur (i.e., sympatry). We then compared the abiotic environment between these three location types and found that sympatry was significantly hotter and drier than the allopatric regions. Thus, sympatry was not intermediate between the alternative allopatric sites. Instead, sympatry occurred at one extreme of the conditions occupied by both species. We hypothesize that biotic interactions in these extreme environments facilitate co-occurrence. Specifically, hybridization between S. bombifrons females and S. multiplicata males may facilitate co-occurrence by decreasing development time of tadpoles. Additionally, the presence of alternative food resources in more extreme conditions may preclude competitive exclusion of one species by the other. This work has implications for predicting how interacting species will respond to climate change, because species interactions may facilitate survival in extreme habitats

Hybridization as a facilitator of species range expansion

Explaining the evolution of species geographical ranges is fundamental to understanding how biodiversity is distributed and maintained. The solution to this classic problem in ecology and evolution remains elusive: we still do not fully know how species geographical ranges evolve and what factors fuel range expansions. Resolving this problem is now more crucial than ever with increasing biodiversity loss, global change and movement of species by humans. Here, we describe and evaluate the hypothesis that hybridization between species can contribute to species range expansion. We discuss how such a process can occur and the empirical data that are needed to test this hypothesis. We also examine how species can expand into new environments via hybridization with a resident species, and yet remain distinct species. Generally, hybridization may play an underappreciated role in influencing the evolution of species ranges. Whether—and to what extent—hybridization has such an effect requires further study across more diverse taxa

Genetic variation during range expansion: effects of habitat novelty and hybridization

How species' ranges evolve remains an enduring problem in ecology and evolutionary biology. Species' range limits are potentially set by the inability of peripheral populations to adapt to range-edge habitat. Indeed, peripheral populations are often assumed to have reduced genetic diversity and population sizes, which limit evolvability. However, support for this assumption is mixed, possibly because the genetic effects of range expansion depend on two factors: the extent that habitat into which expansion occurs is novel and sources of gene flow. Here, we used spadefoot toads, Spea bombifrons, to contrast the population genetic effects of expansion into novel versus non-novel habitat. We further evaluated gene flow from conspecifics and from heterospecifics via hybridization with a resident species. We found that range expansion into novel habitat, relative to non-novel habitat, resulted in higher genetic differentiation, lower conspecific gene flow and bottlenecks. Moreover, we found that hybridizing with a resident species introduced genetic diversity in the novel habitat. Our results suggest the evolution of species' ranges can depend on the extent of differences in habitat between ancestral and newly occupied ranges. Furthermore, our results highlight the potential for hybridization with a resident species to enhance genetic diversity during expansions into novel habitat

Sexual selection's impacts on ecological specialization: an experimental test

In many species, individuals specialize on different resources, thereby reducing competition. Such ecological specialization can promote the evolution of alternative ecomorphs—distinct phenotypes adapted for particular resources. Elucidating whether and how this process is influenced by sexual selection is crucial for understanding how ecological specialization promotes the evolution of novel traits and, potentially, speciation between ecomorphs. We evaluated the population-level effects of sexual selection (as mediated by mate choice) on ecological specialization in spadefoot toad tadpoles that express alternative ecomorphs. We manipulated whether sexual selection was present or reversed by mating females to their preferred versus non-preferred males, respectively. We then exposed their tadpoles to resource competition in experimental mesocosms. The resulting distribution of ecomorphs was similar between treatments, but sexual selection generated poorer trait integration in, and lower fitness of, the more specialized carnivore morph. Moreover, disruptive and directional natural selection were weaker in the sexual selection present treatment. Nevertheless, this effect on disruptive selection was smaller than previously documented effects of ecological opportunity and competitor density. Thus, sexual selection can inhibit adaptation to resource competition and thereby hinder ecological specialization, particularly when females obtain fitness benefits from mate choice that offset the cost of producing competitively inferior offspring

Asymmetric reproductive character displacement in male aggregation behaviour

Reproductive character displacement—the evolution of traits that minimize reproductive interactions between species—can promote striking divergence in male signals or female mate preferences between populations that do and do not occur with heterospecifics. However, reproductive character displacement can affect other aspects of mating behaviour. Indeed, avoidance of heterospecific interactions might contribute to spatial (or temporal) aggregation of conspecifics. We examined this possibility in two species of hybridizing spadefoot toad (genus Spea). We found that in Spea bombifrons sympatric males were more likely than allopatric males to associate with calling males. Moreover, contrary to allopatric males, sympatric S. bombifrons males preferentially associated with conspecific male calls. By contrast, Spea multiplicata showed no differences between sympatry and allopatry in likelihood to associate with calling males. Further, sympatric and allopatric males did not differ in preference for conspecifics. However, allopatric S. multiplicata were more variable than sympatric males in their responses. Thus, in S. multiplicata, character displacement may have refined pre-existing aggregation behaviour. Our results suggest that heterospecific interactions can foster aggregative behaviour that might ultimately contribute to clustering of conspecifics. Such clustering can generate spatial or temporal segregation of reproductive activities among species and ultimately promote reproductive isolation

Widespread disruptive selection in the wild is associated with intense resource competition

Background: Disruptive selection has been documented in a growing number of natural populations. Yet, its prevalence within individual systems remains unclear. Furthermore, few studies have sought to identify the ecological factors that promote disruptive selection in the wild. To address these issues, we surveyed 15 populations of Mexican spadefoot toad tadpoles, Spea multiplicata, and measured the prevalence of disruptive selection acting on resource-use phenotypes. We also evaluated the relationship between the strength of disruptive selection and the intensity of intraspecific competition--an ecological agent hypothesized to be an important driver of disruptive selection. Results: Disruptive selection was the predominant mode of quadratic selection across all populations. However, a directional component of selection favoring an extreme ecomorph -- a distinctive carnivore morph -- was also common. Disruptive selection was strongest in populations experiencing the most intense intraspecific competition, whereas stabilizing selection was only found in populations experiencing relatively weak intraspecific competition. Conclusions: Disruptive selection can be common in natural populations. Intraspecific competition for resources may be a key driver of such selection

Reinforcement generates reproductive isolation between neighbouring conspecific populations of spadefoot toads

Reproductive character displacement is the adaptive evolution of traits that minimize deleterious reproductive interactions between species. When arising from selection to avoid hybridization, this process is referred to as reinforcement. Reproductive character displacement generates divergence not only between interacting species, but also between conspecific populations that are sympatric with heterospecifics versus those that are allopatric. Consequently, such conspecific populations can become reproductively isolated. We compared female mate preferences in, and evaluated gene flow between, neighbouring populations of spadefoot toads that did and did not occur with heterospecifics (mixed- and pure-species populations, respectively). We found that in mixed-species populations females significantly preferred conspecifics. Such females also tended to prefer a conspecific call character that was dissimilar from heterospecifics. By contrast, females from pure-species populations did not discriminate conspecific from heterospecific calls. They also preferred a more exaggerated conspecific call character that resembles heterospecific males. Moreover, gene flow was significantly reduced between mixed- and pure-species population types. Thus, character displacement (and, more specifically, reinforcement) may initiate reproductive isolation between conspecific populations that differ in interactions with heterospecifics

CIRCULAR DICHROISM OF LIGHT-HARVESTING COMPLEXES FROM PURPLE PHOTOSYNTHETIC BACTERIA

The CD spectra of a range of antenna complexes from several different species of purple photosynthetic bacteria were recorded in the wavelength range of 190 to 930 nm. Analysis of the far UV CD (190 to 250 nm) showed that in each case except for the B800-850 from Chr. vinosum the secondary structure of the light-harvesting complexes contains a large amount of α-helix (50%) and very little 0-pleated sheet. This confirms the predictions of the group of Zuber of a high a-helical content based upon consideration of the primary structures of several antenna apoproteins. The CD spectra from the carotenoids and the bacteriochlorophylls show considerable variations depending upon the type of antenna complex. The different amplitude ratios in the CD spectrum for the bacteriochlorophyll Qy, Qx and Soret bands indicate not only different degrees of exciton coupling, but also a strong and variable hyperchromism (Scherz and Parson, 1984a, b)