Emilie C. Snell-Rood

Phenotypic plasticity's impacts on diversification and speciation

Phenotypic plasticity (the ability of a single genotype to produce multiple phenotypes in response to variation in the environment) is commonplace. Yet its evolutionary significance remains controversial, especially in regard to whether and how it impacts diversification and speciation. Here, we review recent theory on how plasticity promotes: (i) the origin of novel phenotypes, (ii) divergence among populations and species, (iii) the formation of new species and (iv) adaptive radiation. We also discuss the latest empirical support for each of these evolutionary pathways to diversification and identify potentially profitable areas for future research. Generally, phenotypic plasticity can play a largely underappreciated role in driving diversification and speciation.

An overview of the evolutionary causes and consequences of behavioural plasticity

I outline how understanding the mechanism of behavioural plasticity is important for predicting how organisms will respond to rapidly changing and novel environments. I define two major forms of behavioural plasticity: developmental and activational. Developmental plasticity refers to the capacity of a genotype to adopt different developmental trajectories in different environments. Activational plasticity refers to differential activation of an underlying network in different environments such that an individual expresses various phenotypes throughout their lifetime. I suggest that the costs and benefits of these two forms of behavioural plasticity may differ: developmental plasticity is slow, but results in a wider range of more integrated responses. Furthermore, the neural costs associated with activational plasticity may be greater because large neural networks must be maintained past an initial sampling and learning phase. While the benefits of plasticity are realized in variable environments, I argue that fine-grained and coarse-grained variation may differentially select for activational and developmental plasticity, respectively. Because environmental variation experienced by an organism is largely determined by behaviour, developmental plasticity may still evolve in fine-grained environments if niche choice results in coarse-grained ‘realized’ variation. Behavioural plasticity should impact evolution in novel environments because it increases the chances of survival in these environments. Developmental behavioural plasticity may be particularly important for diversification in novel environments because it can impact not only survival, but also the development of signals and preferences important in mate choice. Future areas of research on behavioural plasticity and rapid environmental change include stress as a mechanism underlying rapid integrated responses and life history perspectives on predicting developmental versus evolutionary responses.

Toward a population genetic framework of developmental evolution: the costs, limits, and consequences of phenotypic plasticity

Adaptive phenotypic plasticity allows organisms to cope with environmental variability, and yet, despite its adaptive significance, phenotypic plasticity is neither ubiquitous nor infinite. In this review, we merge developmental and population genetic perspectives to explore costs and limits on the evolution of plasticity. Specifically, we focus on the role of modularity in developmental genetic networks as a mechanism underlying phenotypic plasticity, and apply to it lessons learned from population genetic theory on the interplay between relaxed selection and mutation accumulation. We argue that the environmental specificity of gene expression and the associated reduction in pleiotropic constraints drive a fundamental tradeoff between the range of plasticity that can be accommodated and mutation accumulation in alternative developmental networks. This tradeoff has broad implications for understanding the origin and maintenance of plasticity and may contribute to a better understanding of the role of plasticity in the origin, diversification, and loss of phenotypic diversity.

DEVELOPMENTAL DECOUPLING OF ALTERNATIVE PHENOTYPES: INSIGHTS FROM THE TRANSCRIPTOMES OF HORN-POLYPHENIC BEETLES

Developmental mechanisms play an important role in determining the costs, limits, and evolutionary consequences of phenotypic plasticity. One issue central to these claims is the hypothesis of developmental decoupling, where alternate morphs result from evolutionarily independent developmental pathways. We address this assumption through a microarray study that tests whether differences in gene expression between alternate morphs are as divergent as those between sexes, a classic example of developmental decoupling. We then examine whether genes with morph‐biased expression are less conserved than genes with shared expression between morphs, as predicted if developmental decoupling relaxes pleiotropic constraints on divergence. We focus on the developing horns and brains of two species of horned beetles with impressive sexual‐ and morph‐dimorphism in the expression of horns and fighting behavior. We find that patterns of gene expression were as divergent between morphs as they were between sexes. However, overall patterns of gene expression were also highly correlated across morphs and sexes. Morph‐biased genes were more evolutionarily divergent, suggesting a role of relaxed pleiotropic constraints or relaxed selection. Together these results suggest that alternate morphs are to some extent developmentally decoupled, and that this decoupling has significant evolutionary consequences. However, alternative morphs may not be as developmentally decoupled as sometimes assumed and such hypotheses of development should be revisited and refined.

Brain size: a global or induced cost of learning?

The role of brain size as a cost of learning remains enigmatic; the nature and timing of such costs is particularly uncertain. On one hand, comparative studies suggest that congenitally large brains promote better learning and memory. In that case, brain size exacts a global cost that accrues even if learning does not take place; on the other hand, some developmental studies suggest that brains grow with experience, indicating a cost that is induced when learning occurs. The issue of how costs are incurred is an important one, because global costs are expected to constrain the evolution of learning more than would induced costs. We tested whether brain size represented a global and/or an induced cost of learning in the cabbage white butterfly, Pieris rapae. We assayed the ability of full sibling families to learn to locate either green hosts, for which butterflies have an innate search bias, or red hosts, which are more difficult to learn to locate. Naïve butterflies were sacrificed at emergence and congenital brain volume estimated as a measure of global costs; experienced butterflies were sacrificed after learning and change in brain volume estimated as a measure of induced costs. Only for the mushroom body, a brain region involved in learning and memory in other insects, was volume at emergence related to learning or host-finding. Butterfly families that emerged with relatively larger mushroom bodies showed a greater tendency to improve their ability to find red hosts across the two days of host-search. The volume of most brain regions increased with time in a manner suggesting host experience itself was important: first, total number of landings during host-search was positively related to mushroom body calyx volume, and, second, experience with the red host was positively related to mushroom body lobe volume. At the family level, the relative volume of the mushroom body calyx and antennal lobes following learning was positively related to overall success in finding red hosts. Overall, our results suggest that within species, brain size might act as a small global cost of learning, but that environment-specific changes in brain size might reduce the overall costs of neural tissue in the evolution of learning.

Patterns of phenotypic plasticity in common and rare environments: a study of host use and color learning in the cabbage white butterfly Pieris rapae.

Phenotypic plasticity is adaptive in variable environments but, given its costs, may be disfavored if only one environment is commonly encountered. Yet species in relatively constant environments often adjust phenotypes successfully in rare or novel environments. Developmental biases may reduce the costs of plasticity in common environments, favoring the maintenance of plasticity. We explored this proposition by studying the flexibility of visually guided host‐selection behavior in cabbage white butterflies (Pieris rapae), wherein common and rare environments consisted of green and red host types, respectively. We demonstrated in greenhouse assays that adult females display an innate bias toward green color during host search but alter that bias through learning in red‐host assemblages such that, after several hours of experience, red hosts are located as efficiently as green hosts. Full‐sib analyses suggested there was genetic variation in host and color choice that was more pronounced in the red‐host environment. We found no evidence of genetic correlations in behavior across host environments or of fitness costs of plasticity in color choice. Our results support the idea that learning may persist in less variable environments through the evolution of innate biases that reduce operating costs in common environments.

Selective Processes in Development: Implications for the Costs and Benefits of Phenotypic Plasticity

Adaptive phenotypic plasticity, the ability of a genotype to develop a phenotype appropriate to the local environment, allows organisms to cope with environmental variation and has implications for predicting how organisms will respond to rapid, human-induced environmental change. This review focuses on the importance of developmental selection, broadly defined as a developmental process that involves the sampling of a range of phenotypes and feedback from the environment reinforcing high-performing phenotypes. I hypothesize that understanding the degree to which developmental selection underlies plasticity is key to predicting the costs, benefits, and consequences of plasticity. First, I review examples that illustrate that elements of developmental selection are common across the development of many different traits, from physiology and immunity to circulation and behavior. Second, I argue that developmental selection, relative to a fixed strategy or determinate (switch) mechanisms of plasticity, increases the probability that an individual will develop a phenotype best matched to the local environment. However, the exploration and environmental feedback associated with developmental selection is costly in terms of time, energy, and predation risk, resulting in major changes in life history such as increased duration of development and greater investment in individual offspring. Third, I discuss implications of developmental selection as a mechanism of plasticity, from predicting adaptive responses to novel environments to understanding conditions under which genetic assimilation may fuel diversification. Finally, I outline exciting areas of future research, in particular exploring costs of selective processes in the development of traits outside of behavior and modeling developmental selection and evolution in novel environments.

Gene discovery in the horned beetle Onthophagus taurus

BackgroundHorned beetles, in particular in the genus Onthophagus, are important models for studies on sexual selection, biological radiations, the origin of novel traits, developmental plasticity, biocontrol, conservation, and forensic biology. Despite their growing prominence as models for studying both basic and applied questions in biology, little genomic or transcriptomic data are available for this genus. We used massively parallel pyrosequencing (Roche 454-FLX platform) to produce a comprehensive EST dataset for the horned beetle Onthophagus taurus. To maximize sequence diversity, we pooled RNA extracted from a normalized library encompassing diverse developmental stages and both sexes.ResultsWe used 454 pyrosequencing to sequence ESTs from all post-embryonic stages of O. taurus. Approximately 1.36 million reads assembled into 50,080 non-redundant sequences encompassing a total of 26.5 Mbp. The non-redundant sequences match over half of the genes in Tribolium castaneum, the most closely related species with a sequenced genome. Analyses of Gene Ontology annotations and biochemical pathways indicate that the O. taurus sequences reflect a wide and representative sampling of biological functions and biochemical processes. An analysis of sequence polymorphisms revealed that SNP frequency was negatively related to overall expression level and the number of tissue types in which a given gene is expressed. The most variable genes were enriched for a limited number of GO annotations whereas the least variable genes were enriched for a wide range of GO terms directly related to fitness.ConclusionsThis study provides the first large-scale EST database for horned beetles, a much-needed resource for advancing the study of these organisms. Furthermore, we identified instances of gene duplications and alternative splicing, useful for future study of gene regulation, and a large number of SNP markers that could be used in population-genetic studies of O. taurus and possibly other horned beetles.

Insulin signaling as a mechanism underlying developmental plasticity: the role of FOXO in a nutritional polyphenism.

We investigated whether insulin signaling, known to mediate physiological plasticity in response to changes in nutrition, also facilitates discrete phenotypic responses such as polyphenisms. We test the hypothesis that the gene FOXO – which regulates growth arrest under nutrient stress – mediates a nutritional polyphenism in the horned beetle, Onthophagus nigriventris. Male beetles in the genus Onthophagus vary their mating strategy with body size: large males express horns and fight for access to females while small males invest heavily in genitalia and sneak copulations with females. Given that body size and larval nutrition are linked, we predicted that 1) FOXO expression would differentially scale with body size (nutritional status) between males and females, and 2) manipulation of FOXO expression would affect the nutritional polyphenism in horns and genitalia. First, we found that FOXO expression varied with body size in a tissue- and sex-specific manner, being more highly expressed in the abdominal tissue of large (horned) males, in particular in regions associated with genitalia development. Second, we found that knockdown of FOXO through RNA-interference resulted in the growth of relatively larger copulatory organs compared to control-injected individuals and significant, albeit modest, increases in relative horn length. Our results support the hypothesis that FOXO expression in the abdominal tissue limits genitalia growth, and provides limited support for the hypothesis that FOXO regulates relative horn length through direct suppression of horn growth. Both results support the idea that tissue-specific FOXO expression may play a general role in regulating scaling relationships in nutritional polyphenisms by signaling traits to be relatively smaller.

The effect of climate on acoustic signals: Does atmospheric sound absorption matter for bird song and bat echolocation?

The divergence of signals along ecological gradients may lead to speciation. The current research tests the hypothesis that variation in sound absorption selects for divergence in acoustic signals along climatic gradients, which has implications for understanding not only diversification, but also how organisms may respond to climate change. Because sound absorption varies with temperature, humidity, and the frequency of sound, individuals or species may vary signal structure with changes in climate over space or time. In particular, signals of lower frequency, narrower bandwidth, and longer duration should be more detectable in environments with high sound absorption. Using both North American wood warblers (Parulidae) and bats of the American Southwest, this work found evidence of associations between signal structure and sound absorption. Warbler species with higher mean absorption across their range were more likely to have narrow bandwidth songs. Bat species found in higher absorption habitats were more likely to have lower frequency echolocation calls. In addition, bat species changed echolocation call structure across seasons, using longer duration, lower frequency calls in the higher absorption rainy season. These results suggest that signals may diverge along climatic gradients due to variation in sound absorption, although the effects of absorption are modest.