Australian black field crickets show changes in neural gene expression associated with socially-induced morphological, life-history, and behavioral plasticity

Abstract

BackgroundEcological and evolutionary model organisms have provided extensive insight into the ecological triggers, adaptive benefits, and evolution of life-history driven developmental plasticity. Despite this, we still have a poor understanding of the underlying genetic changes that occur during shifts towards different developmental trajectories. The goal of this study is to determine whether we can identify underlying gene expression patterns that can describe the different life-history trajectories individuals follow in response to social cues of competition. To do this, we use the Australian black field cricket (Teleogryllus commodus), a species with sex-specific developmental trajectories moderated by the density and quality of calls heard during immaturity. In this study, we manipulated the social information males and females could hear by rearing individuals in either calling or silent treatments. We next used RNA-Seq to develop a reference transcriptome to study changes in brain gene expression at two points prior to sexual maturation.ResultsWe show accelerated development in both sexes when exposed to calling; changes were also seen in growth, lifespan, and reproductive effort. Functional relationships between genes and phenotypes were apparent from ontological enrichment analysis. We demonstrate that increased investment towards traits such as growth and reproductive effort were often associated with the expression of a greater number of genes with similar effect, thus providing a suite of candidate genes for future research in this and other invertebrate organisms.ConclusionsOur results provide interesting insight into the genomic underpinnings of developmental plasticity and highlight the potential of a genomic exploration of other evolutionary theories such as condition dependence and sex-specific developmental strategies.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3119-y) contains supplementary material, which is available to authorized users.

Direct and indirect effects of sexual signal loss on female reproduction in the Pacific field cricket (Teleogryllus oceanicus)

“…Male T. oceanicus raised in the absence of calling song, mimicking a population with high density of flatwing males or few competitors, invested less in testes size (Bailey et al., ) and exhibit lower sperm viability (Gray & Simmons, ), although acoustic experience does not appear to affect male reproductive success (Heinen‐Kay et al., ). Most studies have found that female crickets reared in the absence of song show reduced investment in reproductive tissues (Bateman, Verburgt, & Ferguson, ; Conroy & Roff, ; Kasumovic, Chen, & Wilkins, ; Kasumovic, Hall, Try, & Brooks, ; Rebar, Barbosa, & Greenfield, ), similar to males, while one study showed no effect of acoustic experience on egg laying (Lierheimer & Tinghitella, ). If experiencing a song‐less environment during rearing is associated with lower reproductive outcomes in T. oceanicus females, sexual signal loss could create a “tragedy of the commons” in which the very trait that benefits males (obligate silence) has negative effects on population fitness through reduced female fecundity (Rankin et al., ).…”

Pre-maturation social experience affects female reproductive strategies and offspring fitness in a highly polyandrous insect

“…Although the precise mechanism underlying this pattern is unknown, previous studies with this species show that females reared in an acoustic environment with variable-quality male calls exhibit several plastic changes when compared with females reared in a silent environment. Some of these changes include the expression of genes associated with energy producing pathways and also higher egg investment (Kasumovic et al 2011(Kasumovic et al , 2016, which could help to understand the results we found here.…”

“…Moreover, male calls experienced by females in early life stages (i.e., pre-maturation) seem to be important for females' reproductive strategies as adults. Females reared in an acoustic environment with variable-quality male calls present a faster antepenultimate development rate, express genes associated with energy producing pathways, and have higher egg investment when compared with females reared in a silent environment (Kasumovic et al 2011(Kasumovic et al , 2016Fig. 1A).…”

Sexual Selection and Extended Phenotypes in Humans

“…Energetic resources during development are also allocated differently depending on the social environment. Males reared under lab conditions in which the density of male calls is higher mature later, are larger, and match their calling to that of the social environment, but die earlier (Kasumovic et al 2016). This plasticity in developmental trajectories, which is associated with trade-offs between mating effort and life history, results in differential gene expression in the brains of male crickets (Kasumovic et al 2016).…”

“…Males reared under lab conditions in which the density of male calls is higher mature later, are larger, and match their calling to that of the social environment, but die earlier (Kasumovic et al 2016). This plasticity in developmental trajectories, which is associated with trade-offs between mating effort and life history, results in differential gene expression in the brains of male crickets (Kasumovic et al 2016). While this level of experimental control and rigour is clearly not possible using human participants, cross-national correlational data are often interpreted as if they were controlled experiments without genetic confounds.…”