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

Abstract

Background: Ecological 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.

Results: We 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.

Conclusions: Our 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.

Keywords: Behaviour; Black field cricket; Developmental plasticity; Gene expression; Sexual selection; Teleogryllus commodus; Transcriptome analysis.

Fig. 1

The difference in the developmental rate (a) and lifespan (b) of males and females reared in the silent and calling treatments. Bars are standard errors

Fig. 2

A heatmap showing the differential gene expression and clustering of samples according to expression values. The samples are on the left axis with notation for the treatments (LV = Low-Variable calling treatment; No = Silent Treatment), Sex (F = Female; M = Male), and age (3 = 3 Days; 13 = 13 Days). The top axis is the gene relationships, and the right axis is the clustering of the samples

Fig. 3

The number of gene ontology (GO) clusters demonstrated to be overexpressed by comparisons between each sex and each treatment within each time period. The GO clusters listed in the figure are GOs that are associated with the regulation of muscle development, molting, metabolic processes, cell development and organization, and molting in the early and late time periods. Each color represents a specific GO cluster. As comparisons are made within each time period, the bars do not represent relative differences in expression between sexes and treatments between time and thus cannot be compared between time periods

Fig. 4

The genes expressed in the different sex (a and b vs. c and d) and calling treatments (a and c vs. b and d) in the different time periods. The red bars represent the number of genes expressed only in that functional group. The blue bars represent the number of genes in that functional group that are also expressed by different groups

Fig. 5

Self-organized maps (SOMs) showing the different expression patterns of the transcription factors expressed by individuals sacrificed at the two time periods: Day3 (a,b) and Day13 (c,d). In both figures, different expression patterns of the transcription factors in individuals of each age group were clustered into 5 × 5 grids by self-organized maps. The expression values are normalised to have a standard deviation of 1. Opposite expression patterns between treatments (Cells 3 and 18 in Early, Cell 1 and 14 in Late) and between sexes (Cells 10 and 16 in Early, Cell 7 and 25 in Late) are extracted and shown to the right of each 5 by 5 grid