Comparative analysis reveals the complex role of histoblast nest size in the evolution of novel insect abdominal appendages in Sepsidae (Diptera)

Abstract

BackgroundThe males of some sepsid species (Sepsidae: Diptera) have abdominal appendages that are remarkable in several ways. They are sexually dimorphic, have a complex evolutionary history of gain and loss, and can be jointed and thus highly mobile. The sternite brushes are used extensively in complex courtship behaviors that differ considerably between species and during mating. The abdominal appendages have a novel developmental pathway developing from histoblast nests rather than imaginal discs.ResultsWe focus on the evolution of cell number, nest area, and segment length in both sexes to understand how this tissue relates to the formation of novel abdominal appendages. We map histoblast nest size of wandering-phase larvae of 17 species across 10 genera to a phylogenetic tree of Sepsidae and demonstrate that abdominal appendages require significant increases of histoblast nest size and cell number in most species while one species produces small appendages even without such modifications. In species with particularly large appendages, not only the nests on the fourth, but nests in neighboring segments are enlarged (Themira biloba, Themira putris). The loss of abdominal appendages corresponds to the loss of an enlarged fourth histoblast nest, although one species showed an exception to this pattern. One species that constitutes an independent origin of abdominal appendages (Perochaeta dikowi) uses an unusual developmental mechanism in that the histoblast nest sizes are not sexually dimorphic.ConclusionsThe surprisingly high diversity in histoblast size and degree of sexual dimorphism suggests that the developmental mechanism used for abdominal appendage formation in sepsids is highly adaptable. The presence of appendages usually correlate with increased histoblast cell number and in most cases appendage loss results in a return to ancestral histoblast morphology. However, we also identify several exceptions that indicate the abdominal appendages have a malleable developmental origin that is responsive to selection.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1265-3) contains supplementary material, which is available to authorized users.

Size rather than complexity of sexual ornaments prolongs male metamorphosis and explains sexual size dimorphism in sepsid flies

“…Thus, any developmental delay signifying a cost of male secondary sexual trait complexity overall appears to be minor in sepsid flies. This may be partially explained by recent findings that merely minor changes in the relative sizes of histoblast nests are required for the development of sternite brushes of very different size [ 57 , 58 ].…”