A morphological trait involved in reproductive isolation between Drosophila sister species is sensitive to temperature

Abstract

Phenotypic plasticity, the capacity of one genotype to generate distinct phenotypes in different environments, is usually thought to facilitate species divergence by opening novel ecological niches to plastic individuals. Here we reveal a case of speciation where this “plasticity first” scenario might not hold. Male genitalia are usually extremely divergent between closely related species, but relatively constant within one species. Under the lock-and-key hypothesis, rapid morphological evolution is associated with a high match between male and female genitalia of the same species and a low match between male and females of closely related species. Previous studies have suggested plasticity of genitalia to be a proof against the lock-and-key hypothesis since the environmentally triggered phenotypic change could modify the “key”. Here we examine the effect of temperature on the shape of the ventral branches, a male genital structure involved in reproductive isolation, in the sister species Drosophila santomea and D. yakuba. We designed a semi-automatic measurement pipeline that can reliably identify curvatures and landmarks based on manually digitized contours of the ventral branches. With this method, we observed that ventral branches are not plastic in D. yakuba but that in D. santomea temperature change phenocopies interspecific genetic variation between both species for ventral branches shape. Our results suggest that speciation of D. santomea and D. yakuba was associated with a gain of plasticity and that genitalia plasticity can be compatible with the lock-and-key hypothesis.

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

“…Previous terminology postgonite posterior paramere (Bock & Wheeler, 1972;Tsacas et al, 1971) dorsal postgonal process dorsal postgonite (Rice et al, 2019;Vincent et al, 2019) dorsal branch (Kamimura, 2010(Kamimura, , 2016Kamimura & Mitsumoto, 2011) dorsal paramere (Bryant & Hsei, 1977) ventral postgonal process ventral postgonite (Rice et al, 2019;Vincent et al, 2019) ventral branch (Kamimura, 2010;Kamimura & Mitsumoto, 2011) ventral paramere (Bryant & Hsei, 1977) aedeagal ventral process phallic spur (Yassin & Orgogozo, 2013) phallic hook (Yassin & Orgogozo, 2013) ventral branch (Kamimura, 2012(Kamimura, , 2016Kamimura & Mitsumoto, 2012b, 2012aA. E. Peluffo et al, 2015;A. Peluffo et al, 2021) aedeagal lateral process basal process (Kamimura, 2007;Kamimura & Polak, 2011) pregonal medial process basal process (Kamimura, 2007), ventral branch (Kamimura, 2016) Postgonal sheath Aedeagal sheath (Rice et al, 2019;Vincent et al, 2019)…”

“…Ventral postgonite (Rice et al, 2019;Vincent et al, 2019) ventral branch (Kamimura & Mitsumoto, 2011;Kamimura, 2010)ventral paramere (Bryant & Hsei, 1977) Aedeagal ventral process Phallic spur (Yassin & Orgogozo, 2013) phallic hook (Yassin & Orgogozo, 2013) ventral branch (Kamimura & Mitsumoto 2012b, 2012aKamimura, 2012Kamimura, , 2016Peluffo et al, 2015Peluffo et al, , 2021 Aedeagal lateral process Basal process (Kamimura & Polak, 2011;Kamimura, 2007) Pregonal medial process Basal process (Kamimura, 2007), ventral branch (Kamimura, 2016) Postgonal sheath Aedeagal sheath (Rice et al, 2019;Vincent et al, 2019) butterflies (Sánchez & Cordero, 2014), or aedeagii of appendicular and non-appendicular origins in bugs and beetles (Aspiras et al, 2011). However, the exact form of selection, for example, cryptic female choice, sexual conflict, and so on, remains debated in the literature (Ah-King et al, 2014;Brennan & Prum, 2015;Eberhard, 1985;Masly, 2012).…”