An innovative ovipositor for niche exploitation impacts genital coevolution between sexes in a fruit-damaging Drosophila

Abstract

Limited attention has been given to ecological factors influencing the coevolution of male and female genitalia. The innovative ovipositor of Drosophila suzukii, an invading fruit pest, represents an appealing case to document this phenomenon. The serrated saw-like ovipositor is used to pierce the hard skin of ripening fruits that are not used by other fruit flies that prefer soft decaying fruits. Here, we highlight another function of the ovipositor related to its involvement in genital coupling during copulation. We compared the morphology and coupling of male and female genitalia in this species to its sibling species, Drosophila subpulchrella, and to an outgroup species, Drosophila biarmipes. These comparisons and a surgical manipulation indicated that the shape of male genitalia in D. suzukii has had to be adjusted to ensure tight coupling, despite having to abandon the use of a hook-like structure, paramere, because of the more linearly elongated ovipositor. This phenomenon demonstrates that ecological niche exploitation can directly affect the mechanics of genital coupling and potentially cause incompatibility among divergent forms. This model case provides new insights towards elucidating the importance of the dual functions of ovipositors in other insect species that potentially induce genital coevolution and ecological speciation.

Limited thermal plasticity and geographic divergence in the ovipositor of Drosophila suzukii

“…One possible explanation for the limited plasticity of the ovipositor could be the effect of stabilizing selection, which could reduce its range of variation. This limited plasticity is congruent with the limited geographic variation detected and previous evidence on coevolution of the ovipositor with the male genitalia (Muto et al, 2018), expected for a trait under stabilizing selection (Eberhard, 2009;Eberhard et al, 1998). A formal Qst/FSt comparison (Ovaskainen et al, 2011) would nevertheless be necessary to test this hypothesis.…”

“…This should be tested experimentally by evaluating the relative performance on a variety of substrates, of the cold and hot-generated ovipositors. Other factors like the existence of alternative selective pressures imposed on the ovipositor morphology such as sexual coevolution (Muto et al, 2018) and pleiotropic genetic effects during the ovipositor development (Green et al, 2018) might limit to such morphological adaptation.…”

Evolution of a pest: towards the complete neuroethology of Drosophila suzukii and the subgenus Sophophora

“…Second, it is also possible that Or85a is only predicted to be a nonfunctional pseudogene from the genomic analyses of D. suzukii due to a premature stop codon. In this case, a shortened sequence for Or85a in D. suzukii might retain functional expression, albeit with a novel ligand spectrum, and thus Or85a acts as a pseudopseudogene, which is a phenomenon that has been previously described in D. melanogaster 53 . However, this has only been documented for an ionotropic glutamate receptor (IR), and the present suggestion would be the first known case of an OR that acts as a pseudo-pseudogene.…”

Female‐driven intersexual coevolution in beetle genitalia

“…Experimental studies imposing different selective regimes have demonstrated that male traits undergo earlier changes within a population relative to females (Cayetano, Maklakov, Brooks, & Bonduriansky, 2011;Wigby & Chapman, 2004), indirectly suggesting a greater influence of selection on males. In contrast, recent studies within populations and between recently diverged species have suggested that novel traits in females may elicit changes in males (Muto et al, 2018;Tanabe & Sota, 2014). However, it remains enigmatic whether any of these processes have played out in any group over long time scales, thereby explaining broad macro-evolutionary patterns of trait diversification.…”