Female-biased population divergence in the venom of the Hentz striped scorpion (Centruroides hentzi)

Abstract

Sex-biased genes are expressed at higher levels in one sex and contribute to phenotypic differences between males and females, as well as overall phenotypic variation within and among populations. Venom has evolved primarily for predation and defense, making venom expression a highly variable phenotype as a result of local adaptation. Several scorpion species have shown both intraspecific and intersexual venom variation, and males have been observed using venom in courtship and mating, suggesting the existence of venom-specific, sex-biased genes that may contribute to population divergence. We used reversed-phase high-performance liquid chromatography (RP-HPLC), Agilent protein bioanalyzer chips, nano-liquid chromatography mass spectrometry (nLC/MS/MS), and median lethal dose (LD) assays in fruit flies (Drosophila melanogaster) and banded crickets (Gryllodes sigillatus) to investigate proteomic and functional venom variation within and among three Florida populations of the Hentz striped scorpion (Centruroides hentzi). We found significant venom variation among populations, with females, not males, being responsible for this divergence. We also found significant variation in venom expression within populations, with males contributing more to within population variation than females. Our results provide evidence that male and female scorpions experience different natural and sexual selective pressures that have led to the expression of sex-biased venom genes and that these genes may be consequential in population divergence.

Insights into how development and life-history dynamics shape the evolution of venom

“…Specifically, females contribute more significantly to the variation of venom between populations. In contrast, within-population venom variation is mostly driven by differences in the venom profile of males [123]. This variation within and among populations is likely contributed in part to sexspecific venom differences.…”

“…The venom profile of the Hentz striped scorpion (Centruroides hentzi) revealed significant intersexual variation within and among populations [123]. Specifically, females contribute more significantly to the variation of venom between populations.…”

“…The majority of studies investigating the sexual dimorphism of venom composition have been reported in scorpions and spiders [39,[120][121][122][123][124][125][126][127]. For example, intersexual variation in venom yield and toxicity has been observed in the Venezuelan scorpion, Tityus nororientalis [128].…”

Evolutionary Ecology of Fish Venom: Adaptations and Consequences of Evolving a Venom System

“…Sexual variation of venom composition has been documented for a few taxa, principally spiders, scorpions, snakes, and a species of fish [122,123,124,125]. Research on Thalassophyrne maculosa (cano toadfish) showed that male venom had double the protein content of that of females and differing bioactivities, with males having a greater target affinity to nociceptors whilst females had greater proteolytic activity [123].…”

Arthropod assassins: Crawling biochemists with diverse toxin pharmacopeias

“…transcriptomic study of a non-buthid scorpion belonging to the family Vaejovidae (Cid-Uribe et al, 2018) and Ward et al examines sex-related differences in the venom composition of the Hentz striped scorpion (Ward et al, 2018a). The remaining reviews do not focus on specific arthropod lineages, but rather provide a general overview of the biochemistry and evolution of arthropod venoms (Laxme et al, 2018) or the structural diversity of arthropod toxins (Daly and Wilson, 2018).…”