Is the morphology of Culicoides intersexes parasitized by mermithid nematodes a parasite adaptation? A morphometric approach to Culicoides circumscriptus (Diptera: Ceratopogonidae)

• A morphometric approach is applied for the first time to Culicoides intersexes.
• The degree of feminization depends on the morphological structure and body size.
• The analyzed dimorphic structures show an intermediate morphology between sexes.
• The wings and antennae are more feminized than the mouthparts.
• Feminized antennae and wings would favor parasite dispersal to infection sites.

Mermithidae is a family of endoparasitic nematodes known to cause intersexuality in arthropods. Intersexes of the genus Culicoides parasitized by mermithids have been the object of several studies aiming to describe their particular morphology. Culicoides intersexes are specimens with male genitalia and feminized sexually dimorphic structures, i.e. antennae, mouthparts and wings. To date, these specimens have only been described qualitatively and a quantitative approach supported by statistical analysis is lacking. Here we conduct morphometric analyses of sexually dimorphic structures in a sample of Culicoides circumscriptus that includes 34 intersexes with the aim of describing precisely the intersexual morphology. The morphology of antennae and the mouthparts was studied by multivariate statistical analysis of linear measures, and wing form by implementing geometric morphometrics techniques. While intersex wings proved to have a similar size to male wings, their shape was intermediate between males and females. However, when allometric shape variation was removed, the wing shape of intersexes was almost identical to that of females. The intersex antennae were morphometrically of the female type, especially when size variation was considered. In contrast, the measured mouthparts (the labrum and the third palpal segment) were halfway between males and females, even when body size was considered. Overall, the antennae and the wings showed a higher degree of feminization than the mouthparts. These findings indicate that the degree of feminization depends both on the morphological structure and on body size. Moreover, we propose that the feminization of the wings and antennae has an adaptive meaning for the parasite, which would favor female-like traits in order to access more easily its breeding sites, where the parasite has plenty of new hosts to infect. Female-like antennae would be beneficial to detect these sites, while having female-like wings would favor the host’s capacity of dispersal to these sites.

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