Resolving between novelty and homology in the rapidly evolving phallus of Drosophila

Rice, Gavin; David, Jean R.; Gompel, Nicolas; Yassin, Amir; Rebeiz, Mark

doi:10.1002/jez.b.23113

Cited by 5 publications

(15 citation statements)

References 81 publications

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“…We see no connection between the base of the pregonites and the claws (figure 1d,e), which confirms that the claws are not 'basal extensions' of the pregonites evident in allied species of the D. ananassae complex [21,25]. The postgonal sheath (sensu [19]) folds and bends freely, and is bilaterally symmetrical, lobe-like and 'cloaks' the claws dorsally (figure 2a-d).…”

Section: Resultssupporting

confidence: 53%

“…Our results provide observational and direct experimental evidence contradicting it: the evidence supports sperm transfer occurring via the route described for other Drosophila, that is, from the aedeagus into the reproductive tract via the female gonopore. Recently, Rice et al [19] showed that the claws have a distinct developmental origin, deriving from the lateral portions of the central primordium of the phallus observable during pupal metamorphosis. Since most cells of the central primordium normally give rise to the aedeagus, the term aedeagal lateral processes for the claw-like structures was proposed [19], a term we adopt here and use interchangeably with 'claws'.…”

Section: Introductionmentioning

confidence: 99%

“…Recently, Rice et al [19] showed that the claws have a distinct developmental origin, deriving from the lateral portions of the central primordium of the phallus observable during pupal metamorphosis. Since most cells of the central primordium normally give rise to the aedeagus, the term aedeagal lateral processes for the claw-like structures was proposed [19], a term we adopt here and use interchangeably with 'claws'. Historically, the claws were thought to be arms of a bifid aedeagus [11,[20][21][22][23] and were termed 'basal processes' by Kamimura [10].…”

Section: Introductionmentioning

confidence: 99%

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Refutation of traumatic insemination in the Drosophila bipectinata species complex

Polák

McEvey

2022

Biol. Lett.

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Traumatic insemination (TI) is a rare reproductive behaviour characterized by the transfer of sperm to the female via puncture wounds inflicted across her body wall. Here, we challenge the claim made by Kamimura (Kamimura 2007 Biol. Lett. 3 , 401–404. ( doi:10.1098/rsbl.2007.0192 )) that males of species of the Drosophila bipectinata complex use a pair of claw-like processes (claws) to traumatically inseminate females: the claws are purported to puncture the female body wall and genital tract, and to inject sperm through the wounds into the lumen of her genital tract, bypassing the vaginal opening. This supposed case of TI is widely cited and featured in prominent subject reviews. We examined high-resolution scanning electron micrographs of the claws and failed to discover any obvious ‘groove’ for sperm transport. We demonstrated that sperm occurred in the female reproductive tract as a single-integrated unit, inconsistent with the claim that sperm are injected via paired processes. Laser ablation of the sharp terminal ends of the claws failed to inhibit insemination. We showed that the aedeagus in the complex delivers sperm through the vaginal opening, as in other Drosophila . The results refute the claim of TI in the Drosophila bipectinata species complex.

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Section: Resultssupporting

confidence: 53%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Refutation of traumatic insemination in the Drosophila bipectinata species complex

Polák

McEvey

2022

Biol. Lett.

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“…We confirmed the presence of Svb in the inner cavity of the developing ovipositors of D. melanogaster and the sha expression in the similar regions of D. suzukii and D. subpulchrella , suggesting that the network is also utilized to develop the ovipositor trichomes. Taken together, in parallel to the well-documented cases of rapidly evolving genital structures in Drosophila males (e.g., [ 42 – 45 ]), our study opens an opportunity to explore the evolution of a rapidly diversifying morphological trait of the female genitalia. Our study also highlights the gene regulatory network of a functionally distinct and divergent trichome system associated with ecological niche exploitation.…”

Section: Discussionsupporting

confidence: 57%

Trichomes on female reproductive tract: rapid diversification and underlying gene regulatory network in Drosophila suzukii and its related species

et al. 2022

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Background The ovipositors of some insects are external female genitalia, which have their primary function to deliver eggs. Drosophila suzukii and its sibling species D. subpulchrella are known to have acquired highly sclerotized and enlarged ovipositors upon their shifts in oviposition sites from rotting to ripening fruits. Inside the ovipositor plates, there are scale-like polarized protrusions termed “oviprovector scales” that are likely to aid the mechanical movement of the eggs. The size and spatial distribution of the scales need to be rearranged following the divergence of the ovipositors. In this study, we examined the features of the oviprovector scales in D. suzukii and its closely related species. We also investigated whether the scales are single-cell protrusions comprised of F-actin under the same conserved gene regulatory network as the well-characterized trichomes on the larval cuticular surface. Results The oviprovector scales of D. suzukii and D. subpulchrella were distinct in size and spatial arrangement compared to those of D. biarmipes and other closely related species. The scale numbers also varied greatly among these species. The comparisons of the size of the scales suggested a possibility that the apical cell area of the oviprovector has expanded upon the elongation of the ovipositor plates in these species. Our transcriptome analysis revealed that 43 out of the 46 genes known to be involved in the trichome gene regulatory network are expressed in the developing female genitalia of D. suzukii and D. subpulchrella. The presence of Shavenbaby (Svb) or svb was detected in the inner cavity of the developing ovipositors of D. melanogaster, D. suzukii, and D. subpulchrella. Also, shavenoid (sha) was expressed in the corresponding patterns in the developing ovipositors and showed differential expression levels between D. suzukii and D. subpulchrella at 48 h APF. Conclusions The oviprovector scales have divergent size and spatial arrangements among species. Therefore, these scales may represent a rapidly diversifying morphological trait of the female reproductive tract reflecting ecological contexts. Furthermore, our results showed that the gene regulatory network underlying trichome formation is also utilized to develop the rapidly evolving trichomes on the oviprovectors of these flies.

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“…For this reason, they are excellent candidates for genetic and developmental investigations of novel traits. As an example, diverse genital morphologies are present in species of Drosophila , and the rapid pace of genital evolution has often been attributed to conflict between the sexes [18], [19], [21]. Drosophila eugracilis ( D .…”

Section: Introductionmentioning

confidence: 99%

Gene regulatory network co-option is sufficient to induce a morphological novelty inDrosophila

Rice,

Gaitan-Escudero,

Charles-Obi

et al. 2024

Preprint

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Identifying the molecular origins by which new morphological structures evolve is one of the long standing problems in evolutionary biology. To date, vanishingly few examples provide a compelling account of how new morphologies were initially formed, thereby limiting our understanding of how diverse forms of life derived their complex features. Here, we provide evidence that the large projections on the Drosophila eugracilis phallus that are implicated in sexual conflict have evolved through co-option of the trichome genetic network. These unicellular apical projections on the phallus postgonal sheath are reminiscent of trichomes that cover the Drosophila body but are up to 20-fold larger in size. During their development, they express the transcription factor Shavenbaby, the master regulator of the trichome network. Consistent with the co-option of the Shavenbaby network during the evolution of the D. eugracilis projections, somatic mosaic CRISPR/Cas9 mutagenesis shows that shavenbaby is necessary for their proper length. Moreover, mis-expression of Shavenbaby in the sheath of D. melanogaster, a naive species that lacks these extensions, is sufficient to induce small trichomes. These induced extensions rely on a genetic network that is shared to a large extent with the D. eugracilis projections, indicating its co-option but also some genetic rewiring. Thus, by leveraging a genetically tractable evolutionarily novelty, our work shows that the trichome-forming network is flexible enough that it can be co-opted in a new context, and subsequently refined to produce unique apical projections that are barely recognizable compared to their simpler ancestral beginnings.

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Resolving between novelty and homology in the rapidly evolving phallus of Drosophila

Cited by 5 publications

References 81 publications

Refutation of traumatic insemination in the Drosophila bipectinata species complex

Refutation of traumatic insemination in the Drosophila bipectinata species complex

Trichomes on female reproductive tract: rapid diversification and underlying gene regulatory network in Drosophila suzukii and its related species

Gene regulatory network co-option is sufficient to induce a morphological novelty inDrosophila

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