Resolving Between Novelty and Homology in the Rapidly Evolving Phallus of Drosophila

Abstract

The genitalia present some of the most rapidly evolving anatomical structures in the animal kingdom, possessing a variety of parts that can distinguish recently diverged species. In the Drosophila melanogaster group, the phallus is adorned with several processes, pointed outgrowths, that are similar in size and shape between species. However, the complex three-dimensional nature of the phallus can obscure the exact connection points of each process. Previous descriptions based upon adult morphology have primarily assigned phallic processes by their approximate positions in the phallus and have remained largely agnostic regarding their homology relationships. In the absence of clearly identified homology, it can be challenging to model when each structure first evolved. Here, we employ a comparative developmental analysis of these processes in eight members of the melanogaster species group to precisely identify the tissue from which each process forms. Our results indicate that adult phallic processes arise from three pupal primordia in all species. We found that in some cases the same primordia generate homologous structures whereas in other cases, different primordia produce phenotypically similar but remarkably non-homologous structures. This suggests that the same gene regulatory network may have been redeployed to different primordia to induce phenotypically similar traits. Our results highlight how traits diversify and can be redeployed, even at short evolutionary scales.

Refutation of traumatic insemination in the Drosophila bipectinata species complex: Hypothesis fails critical tests

“…Our results provide observational and direct experimental evidence contradicting such a claim: the evidence supports sperm transfer occurring via the route of sperm delivery in other Drosophila, that is, through the female gonopore into the reproductive tract. In the present section we first offer a reinterpretation of the male phallic architecture of species within the bipectinata complex, following the standardized nomenclature proposed for D. melanogaster (Rice et al, 2019) and refined for a wider group of species following developmental studies (Rice et al, 2021). On the one hand, we agree with K2007 that the paired claw-like structures, the purported piercing organs of TI, are not a "bifid aedeagus", a terminology adopted by earlier authors.…”

“…They are bilaterally symmetrical, and arise from the lateral portions ("shoulders") (Fig. 2A, D, E), not the center, of the apex of the phallapodeme (this comports with the ontogeny described by Rice et al, 2021).…”

“…The phallic structures of the bipectinata complex are represented here by D. bipectinata and D. parabipectinata; the same, or very similar, morphology is present in the other two species of the bipectinata complex (Bock, 1971). Naming the parts of the copulatory apparatus is difficult because they are exceptionally evolutionary labile, their homologies obscure (but see Rice et al, 2021), and their function often speculative.…”

“…malerkotliana Parshad and Paika, 1965;and D. pseudoananassae Bock, 1971 (Bock, 1971). Specifically, males of these species are purported to use a pair of claw-like phallic structures, called "basal processes" by K2007, but which we call aedeagal lateral processes following Rice et al (2021), as explained below, to pierce the female body wall and reproductive tract, and inject sperm into her reproductive tract through the wound sites. If true, then TI in this complex would be an astonishing evolutionary innovation within the genus, family and order.…”

“…On the other hand, we also agree with Rice et al 's (2021) suggestion that the claw-like structures should be termed "aedeagal lateral processes", rather than K2007's "basal processes". Rice et al (2021) showed that the claws have a distinct developmental origin, deriving from the lateral portions of the central primordium of the phallus observable during metamorphosis in the pupa. Since most of the cells of the central primordium normally give rise, in related Drosophila subgroups, to the aedeagus (not to postgonites, pregonites, or postgonal sheath) the term aedeagal lateral process was proposed by Rice et al (2021), a term we adopt here.…”