Signals of selection in conditionally expressed genes in the diversification of three horned beetle species.

Species radiations may be facilitated by phenotypic differences already present within populations, such as those arising through sex-specific development or developmental processes biased towards particular reproductive or trophic morphs. We sought to test this hypothesis by utilizing a comparative transcriptomic approach to contrast among- and within-species differentiation using three horned beetle species in the genus Onthophagus. These three species exhibit differences along three phenotypic axes reflective of much of the interspecific diversity present within the genus: horn location, polarity of sexual dimorphism and degree of nutritional sensitivity. Our approach combined de novo transcript assembly, assessment of amino acid substitutions (dN/dS) across orthologous gene pairs and integration of gene function and conditional gene expression data. We identified 17 genes across the three species pairs related to axis patterning, development and metabolism with dN/dS > 1 and detected elevated dN/dS in genes related to metabolism and biosynthesis in the most closely related species pair, which is characterized by a loss of nutritional polyphenism and a reversal of sexual dimorphism. Further, we found that genes that are conditionally expressed (i.e. as a function of sex, nutrition or body region) within one of our focal species also showed significantly stronger signals of positive or relaxed purifying selection between species divergent along the same morphological axis (i.e. polarity of sexual dimorphism, degree of nutritional sensitivity or location of horns). Our findings thus reveal a positive relationship between intraspecific differentiation due to condition-specific development and genetic divergences among species.

Asymmetric interactions between doublesex and tissue- and sex-specific target genes mediate sexual dimorphism in beetles.

Sexual dimorphisms fuel significant intraspecific variation and evolutionary diversification. Yet the developmental-genetic mechanisms underlying sex-specific development remain poorly understood. Here, we focus on the conserved sex-determination gene doublesex (dsx) and the mechanisms by which it mediates sex-specific development in a horned beetle species by combining systemic dsx knockdown, high-throughput sequencing of diverse tissues and a genome-wide analysis of Dsx-binding sites. We find that Dsx regulates sex-biased expression predominantly in males, that Dsx's target repertoires are highly sex- and tissue-specific and that Dsx can exercise its regulatory role via two distinct mechanisms: as a sex-specific modulator by regulating strictly sex-specific targets, or as a switch by regulating the same genes in males and females in opposite directions. More generally, our results suggest Dsx can rapidly acquire new target gene repertoires to accommodate evolutionarily novel traits, evidenced by the large and unique repertoire identified in head horns, a recent morphological innovation.

Developmental plasticity and evolution--quo vadis?

The role of developmental (phenotypic) plasticity in ecology and evolution is receiving a growing appreciation among the biologists, and many plasticity-specific concepts have become well established as part of the mainstream evolutionary biological thinking. In this essay, I posit that despite this progress several key perspectives in developmental plasticity remain remarkably traditional, and that it may be time to re-evaluate their continued usefulness in the face of the available evidence as the field looks to its future. Specifically, I discuss the utility of viewing plastic development as ultimately rooted in genes and genomes, and investigate the common notion that the environment--albeit a critical source of information--nevertheless remains passive, external to and separable from the organism responding to it. I end by highlighting conceptual and empirical opportunities that may permit developmental plasticity research to transcend its current boundaries and to continue its contributions toward a holistic and realistic understanding of organismal development and evolution.

On the origins of novelty and diversity in development and evolution: a case study on beetle horns.

The origin of novel features continues to represent a major frontier in evolutionary biology. What are the genetic, developmental, and ecological processes that mediate not just the modification of preexisting traits, but the origin of novel traits that lack obvious homology with other structures? In this chapter, I highlight a class of traits and organisms that are emerging as new models for exploring the mechanisms of innovation and diversification in nature: beetle horns and horned beetles. Here, I review recent significant findings and their contributions to current frontiers in evolutionary developmental biology.

Integrating micro- and macroevolution of development through the study of horned beetles.

A major challenge in evolutionary developmental biology is to understand how developmental evolution on the level of populations and closely related species relates to macroevolutionary transitions and the origin of evolutionary novelty. Here, I review the genetic, developmental, endocrine, and ecological basis of beetle horns, a morphological novelty that exhibits remarkable diversity both below and above the species level. Integrating from a variety of approaches three major insights emerge: the origin of beetle horns relied at least in part on the redeployment of already existing genetic, developmental and endocrine mechanisms. At the same time little to no phylogenetic distance appeared to have been necessary for the evolution of diverse modifier mechanisms that permit substantial modulation of trait expression at different time points during development in different species, sexes, alternative male morphs or even different tissue regions of the same individual. Lastly, at least a subset of these modifier mechanisms can evolve rapidly in geographically isolated populations, apparently driven by relatively simple, and probably ubiquitous, changes in ecological conditions. I discuss the implications of these results for our understanding of the genesis of morphological novelty and diversity.