Distinct developmental mechanisms underlie the evolutionary diversification of Drosophila sex combs

Abstract

Similar selective pressures can lead to independent origin of similar morphological structures in multiple evolutionary lineages. Developmental mechanisms underlying convergent evolution remain poorly understood. In this report, we show that similar sex comb morphology in closely related Drosophila species is produced by different cellular mechanisms. The sex comb is a recently evolved, male-specific array of modified bristles derived from transverse bristle rows found on the first thoracic legs in both sexes. ''Longitudinal'' sex combs oriented along the proximo-distal leg axis evolved independently in several Drosophila lineages. We show that in some of these lineages, sex combs originate as one or several transverse bristle rows that subsequently rotate 90°and align to form a single longitudinal row. In other species, bristle cells that make up the sex combs arise in their final longitudinal orientation. Thus, sex combs can develop through either sexspecific patterning of bristle precursor cells or male-specific morphogenesis of sexually monomorphic precursors. Surprisingly, the two mechanisms produce nearly identical morphology in some species. Phylogenetic analysis shows that each of these mechanisms has probably evolved repeatedly in different Drosophila lineages, suggesting that selection can recruit different cellular processes to produce similar functional solutions. Convergent evolution ͉ Morphogenesis ͉ Sexual dimorphism

Evolution of Drosophila sex comb length illustrates the inextricable interplay between selection and variation

“…6C and 8E). In some species, multiple small sex combs rotate and fuse such as in the t2 of D. rhopaloa (22) and Lordiphosa magnipectinata (25), potential obstacles are not only absent, but are replaced by additional sex combs (Fig. 8F).…”

“…8F). Finally, nonrotating vertical sex combs derived from longitudinal row bristles suggest an alternative developmental strategy to permit large combs with apparently fewer spatial limitations than those encountered when modifying transverse row bristles into combs (22,25) (Fig. 8G).…”

“…As with many secondary sexual traits, over a relatively short timescale, sex combs have evolved great pattern diversity between species including different numbers of bristles per comb and various degrees of bristle pigmentation (17,18,22,23). In particular, sex comb length displays a high level of variation across Drosophila species, and has increased and decreased repeatedly during evolution (17,18,22,23) (Supporting Information, Fig.…”

“…In particular, sex comb length displays a high level of variation across Drosophila species, and has increased and decreased repeatedly during evolution (17,18,22,23) (Supporting Information, Fig. S1) (Any mention in this paper regarding sex comb length strictly refers to bristle number per comb).…”

Evolution of sex comb from the primitive bristle pattern in drosophila is associated with modification in the developmental regulatory protein dachshund

“…In species which have sex comb, it has been shown to provide better grasping during mating, and thereby increase the selective fitness of the male (Markow et al, 1996;Polak et al, 2004;Spieth, 1952). The ability of making a sex comb from the primitive transverse row of bristles (Tokunaga, 1962) requires two important changes in patterning, Viz: heavy chitinization of the bristles to transform them into teeth, and rotation of the row of transverse bristles to make it more longitudinal to the axis of the leg as in case of Drosophila melanogaster (Atallah et al, 2009;Held et al, 2004;Tanaka et al, 2009). These phenotypic alterations, resulting in the evolution of the sex comb should be an outcome of crucial and parallel changes in the genetic network regulating the developmental programme of the formation of the ancestral transverse bristles pattern on the prothoracic tarsal segments.…”