Molecular and Developmental Signatures of Genital Size Macro-Evolution in Bugs.

Our understanding of the genetic architecture of phenotypic traits has experienced drastic growth over the last years. Nevertheless, the majority of studies associating genotypes and phenotypes have been conducted at the ontogenetic level. Thus, we still have an elusive knowledge of how these genetic-developmental architectures evolve themselves and how their evolution is mirrored in the phenotypic change across evolutionary time. We tackle this gap by reconstructing the evolution of male genital size, one of the most complex traits in insects, together with its underlying genetic architecture. Using the order Hemiptera as a model, spanning over 350 million years of evolution, we estimate the correlation between genitalia and three features: development rate, body size, and rates of DNA substitution in 68 genes associated with genital development. We demonstrate that genital size macro-evolution has been largely dependent on body size and weakly influenced by development rate and phylogenetic history. We further revealed significant correlations between mutation rates and genital size for 19 genes. Interestingly, these genes have diverse functions and participate in distinct signaling pathways, suggesting that genital size is a complex trait whose fast evolution has been enabled by molecular changes associated with diverse morphogenetic processes. Our data further demonstrate that the majority of DNA evolution correlated with the genitalia has been shaped by negative selection or neutral evolution. Thus, in terms of sequence evolution, changes in genital size are predominantly facilitated by relaxation of constraints rather than positive selection, possibly due to the high pleiotropic nature of the morphogenetic genes.

Comparative morphology of clasping structures in predator stink bugs (Hemiptera: Pentatomidae: Asopinae): Insights into their function and evolution.

Parameres are male genital structures found in many insects which are often used as clasping devices to exert dominance in copula. The asopines have evolved a remarkable additional pair of similar structures, often denominated processes, which combines with the parameres in a tweezers-like system. Processes in similar positions have also been found in other subfamilies of Pentatomidae, but smaller and less developed. Using scanning electron microscopy, we document the among-species variability found in the clasping structures in asopines. We first revealed a vast diversity of ornamentations, such as sensilla and microsculpture. When present, these ornamentations are invariably found on both, the parameres and processes, and often on the corresponding female parts, the valvifers VIII, indicating a functional role of attachment and sensory perception in copula for the ornamentations. We also show that the processes are drastically different between the Asopinae and non-asopines. Therefore, we suggest the term "pseudoclasper" for the Asopinae processes and "superior process of dorsal rim" for the remaining examined taxa. The pseudoclaspers are directly connected to and attached in the same place as the parameres in asopines, while the superior processes of dorsal rim and parameres are completely disconnected in other pentatomids. These results indicate a non-homologous origin between pseudoclaspers and superior processes of dorsal rim in Pentatomidae.

Copulatory function and development shape modular architecture of genitalia differently in males and females.

Genitalia are multitasking structures whose development is mediated by numerous regulatory pathways. This multifactorial nature provides an avenue for multiple sources of selection. As a result, genitalia tend to evolve as modular systems comprising semi-independent subsets of structures, yet the processes that give rise to those patterns are still poorly understood. Here, we ask what are the relative roles of development and function in shaping modular patterns of genitalia within populations and across species of stink-bugs. We found that male genitalia are less integrated, more modular, and primarily shaped by functional demands. In contrast, females show higher integration, lower modularity, and a predominant role of developmental processes. Further, interactions among parts of each sex are more determinant to modularity than those between the sexes, and patterns of modularity are equivalent between and within species. Our results strongly indicate that genitalia have been subjected to sex-specific selection, although male and female genitalia are homologous and functionally associated. Moreover, modular patterns are seemingly constant in the evolutionary history of stink-bugs, suggesting a scenario of multivariate stabilizing selection within each sex. Our study demonstrates that interactions among genital parts of the same sex may be more fundamental to genital evolution than previously thought.

Female-driven intersexual coevolution in beetle genitalia.

Genital coevolution is a pervasive phenomenon as changes in one sex tend to impose fitness consequences on the other, generating sexual conflict. Sexual conflict is often thought to cause stronger selection on males due to the Darwin-Bateman's anisogamy paradigm. However, recent studies have demonstrated that female genitalia may be equally elaborated and perform diverse extra-copulatory functions. These characteristics suggest that female genitals can also be primary targets of selection, especially where natural selection acts on female-exclusive functions such as oviposition. Here, we test this hypothesis in a statistical phylogenetic framework across the whole beetle (Coleoptera) phylogeny, investigating whether coevolution of specific genital traits may be triggered by changes in females. We focus on traits of the proctiger, which composes part of the male terminalia and the female ovipositor. Our results present a comprehensive case of male-female genital coevolution and provide solid statistical evidence for a female-initiated coevolutionary process where the vast majority of evolutionary transitions in males have occurred only after changes in females. We corroborate the hypothesis that female traits may change independently and elicit counter-adaptations in males. Furthermore, by showing a consistent pattern across the phylogeny of the most diverse group of animals, our results suggest that this female-driven dynamics may persist through long time scales.

De novo construction of a transcriptome for the stink bug crop pest Chinavia impicticornis during late development.

Chinavia impicticornis is a neotropical stink bug of economic importance for various crops. Little is known about the development of the species, or the genetic mechanisms that may favor the establishment of populations in cultivated plants. Here, we conduct the first large-scale molecular study of C. impicticornis. Using tissues derived from the genitalia and the rest of the body for two immature stages of both males and females, we generated RNA-seq data, then assembled and functionally annotated a transcriptome. The de novo-assembled transcriptome contained around 400,000 contigs, with an average length of 688 bp. After pruning duplicated sequences and conducting a functional annotation, the final annotated transcriptome comprised 39,478 transcripts, of which 12,665 were assigned to Gene Ontology (GO) terms. These novel datasets will be invaluable for the discovery of molecular processes related to morphogenesis and immature biology. We hope to contribute to the growing body of research on stink bug evolution and development, as well as to the development of biorational pest management solutions.

Review and phylogeny of the geniculata group, genus Chinavia (Heteroptera: Pentatomidae), with notes on biogeography and morphological evolution.

Chinavia is one of the most diverse genera of Pentatomidae, comprising 80 species distributed in the Afrotropical, Neartic and Neotropical regions. Some groups of species have been proposed in the literature based on morphological similarities or phylogenetic analyses. The geniculata group was proposed to include C. geniculata, C. gravis and C. nigritarsis. However, eleven other species of Chinavia share somatic and genital characteristics with C. geniculata, C. gravis and C. nigritarsis, which allows hypothesizing the monophyly among these 14 species. In spite of the recent contributions to aspects of biology, immature stages and species catalogs in Chinavia, the definition of monophyletic groups within the genus and the establishment of boundaries among its species are essential to understand its diversity and to test hypotheses on biogeography and evolutionary biology. In this study we review the taxonomy of the geniculata group, test its monophyly and propose a phylogenetic hypothesis for the group. We discuss the phylogenetic relationships from a geographical perspective, and provide insights about morphological evolution.