Sex-specific expression of a HOX gene associated with rapid morphological evolution

Abstract

Animal diversity is shaped by the origin and diversification of new morphological structures. Many examples of evolutionary innovations are provided by male-specific traits involved in mating and sexual selection. The origin of new sex-specific characters requires the evolution of new regulatory interactions between sex-determining genes and genes that control spatial patterning and cell differentiation. Here, we show that sex-specific regulation of the HOX gene Sex combs reduced (Scr) is associated with the origin and evolution of the Drosophila sex comb - a novel and rapidly diversifying male-specific organ. In species that primitively lack sex combs, Scr expression shows little spatial modulation, whereas in species that have sex combs, Scr is upregulated in the presumptive sex comb region and is frequently sexually dimorphic. Phylogenetic analysis shows that sex-specific regulation of Scr has been gained and lost multiple times in Drosophila evolution and correlates with convergent origin of similar sex comb morphologies in several independent lineages. Some of these transitions occurred on microevolutionary timescales, indicating that HOX gene expression can evolve with surprising ease. This is the first example of a sex-specific regulation of a HOX gene contributing to the development and evolution of a secondary sexual trait.

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

“…Rest of the members of Drosophilidae have the basic pattern of transverse rows of bristles on tibia and the first tarsal segments (ts1) of the prothoracic legs, which is the same as what is seen on the legs of the females of all Drosophila species (Fig. 1b) (Barmina and Kopp, 2007;Kopp and True, 2002). Sex comb is usually represented by array of one or few rows of chitinized teeth in the proximal tarsal segments of the prothoracic leg (Fig.…”

“…dachshund gain of function results in ectopic expression of SCR in second tarsal segment (ts2) of prothoracic leg and formation of distal additional sex comb in D. melanogaster and bab loss of function mutants have a similar effect, indicating that DAC acts as an activator whereas BAB acts as a genetic repressor of Scr during sex comb development (Randsholt and Santamaria, 2008). Earlier studies within Sophophora subgenus have shown that the sex comb diversity is not associated with any corresponding variation in expression patterns of DAC and BAB in the prothoracic leg discs among different species (Barmina and Kopp, 2007;Randsholt and Santamaria, 2008).…”

“…The strong SCR expression in ts1 and ts2 is characteristic feature of the species with sex comb and is secondarily lost in those species of Sophophora, which have lost sex comb later during evolution. It is important to note that, these secondary loses/gains of sex combs within the melanogaster species group are not associated with changes in DAC expression (Barmina and Kopp, 2007;Randsholt and Santamaria, 2008).…”

“…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. Having acquired the potential of making this new morphological structure, flies in the Sophophora clad have secondarily undergone extraordinary degree of diversification with respect to this trait, exhibiting variations in comb and teeth number and their arrangement (Barmina and Kopp, 2007;Lemeunier et al, 1986;Randsholt and Santamaria, 2008).…”

“…Studies in the species of Sophophora group (Barmina and Kopp, 2007;Kopp, 2011;Randsholt and Santamaria, 2008) have shown that within the sub-genus, variations in the sex comb morphology, are strongly correlated with a modulation in spatial and quantitative expression of homeotic gene Sex combs reduced (Scr) in the 1st and 2nd tarsal segments of the prothoracic leg discs of male Drosophila. Loss and gain of this morphological structure in different species among Sophophora has been strictly correlated to the loss or gain and alterations in expression of SCR in the tarsal segments.…”