Diversification through gustatory courtship: an X-ray micro-computed tomography study on dwarf spiders

BACKGROUND: Sexual selection has been considered to promote diversification and speciation. Sexually dimorphic species have been used to explore the supposed effect, however, with mixed results. In dwarf spiders (Erigoninae), many species are sexually dimorphic—males possess marked prosomal modifications. These male traits vary from moderate elevations to bizarre shapes in various prosomal regions. Previous studies established that male dwarf spiders produce substances in these prosomal modifications that are taken up by the females. These substances can act as nuptial gifts, which increase the mating probability of males and the oviposition rate in females. Therefore, these dimorphic traits have evolved in the context of sexual selection. Here, we explore the evolutionary lability of this gustatory trait complex with the aim of assessing the role of this trait complex in species divergence by investigating (1) if erigonine modified prosomata are inherently linked to nuptial-gift-producing glands, (2) if the evolution of the glands evolution preceded that of the modified prosomal shapes, and by assessing (3) the occurrence of convergent/divergent evolution and cryptic differentiation. RESULTS: We reconstructed the position and extent of the glandular tissue along with the muscular anatomy in the anterior part of the prosoma of 76 erigonine spiders and three outgroup species using X-ray micro-computed tomography. In all but one case, modified prosomata are associated with gustatory glands. We incorporated the location of glands and muscles into an existing matrix of somatic and genitalic morphological traits of these taxa and reanalyzed their phylogenetic relationship. Our analysis supports that the possession of glandular equipment is the ancestral state and that the manifold modifications of the prosomal shape have evolved convergently multiple times. We found differences in gland position between species with both modified and unmodified prosomata, and reported on seven cases of gland loss. CONCLUSIONS: Our findings suggest that the occurrence of gustatory glands in sexually monomorphic ancestors has set the stage for the evolution of diverse dimorphic external modifications in dwarf spiders. Differences among congeners suggest that the gland position is highly susceptible to evolutionary changes. The multiple incidences might reflect costs of glandular tissue maintenance and nuptial feeding. Our results indicate divergent evolutionary patterns of gustatory-courtship-related traits, and thus a likely facilitating effect of sexual selection on speciation. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12983-021-00435-8.