Orthology, Function and Evolution of Accessory Gland Proteins in the Drosophila Repleta Group

By Almeida, Francisca C.; DeSalle, Rob | Genetics, January 2009 | Go to article overview
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Orthology, Function and Evolution of Accessory Gland Proteins in the Drosophila Repleta Group


Almeida, Francisca C., DeSalle, Rob, Genetics


ABSTRACT

The accessory gland proteins (Acps) of Drosophila have become a model for the study of reproductive protein evolution. A major step in the study of Acps is to identify biological causes and consequences of the observed patterns of molecular evolution by comparing species groups with different biology. Here we characterize the Acp complement of Drosophila mayaguana, a repleta group representative. Species of this group show important differences in ecology and reproduction as compared to other Drosophila. Our results show that the extremely high rates of Acp evolution previously found are likely to be ubiquitous among species of the repleta group. These evolutionary rates are considerably higher than the ones observed in other Drosophila groups' Acps. This disparity, however, is not accompanied by major differences in the estimated number of Acps or in the functional categories represented as previously suggested. Among the genes expressed in accessory glands of D. mayaguana almost half are likely products of recent duplications. This allowed us to test predictions of the neofunctionalization model for gene duplication and paralog evolution in a more or less constrained timescale. We found that positive selection is a strong force in the early divergence of these gene pairs.

ACCESSORY gland proteins (Acps) are secreted by the accessory glands of Drosophila males during insemination and perform fundamental roles in reproduction, being essential for egg fertilization (for reviews, see Wolfner 2002 and Chapman and Davies 2004). Comparisons between Drosophila simulans and D. melanogaster orthologs showed that Acps on average have two times more replacement substitutions than non-Acp genes (Swanson et al. 2001). Rapid evolution and high turnover rates of Acps result in the observation that the more phylogenetically distant two species are, the more difficult it is to identify Acp orthologs in their genomes (Haerty et al. 2007). For example, of 52 Acps identified in D. melanogaster, only 29 had detectable orthologs in the D. pseudoobscura genome(Mueller et al. 2005), while all 52 Acps are present in D. simulans, a species closely related to D. melanogaster (but see also Begun and Lindfors 2005). These and other studies on the melanogaster and pseudoobscura groups showed that Acps are frequently subject to gene duplication and gene loss (Begun and Lindfors 2005; Wagstaff and Begun 2005a).

The melanogaster group, on which most of the Acp studies have been focused, represents only a small sample of theDrosophila genus.Drosophila encompasses a large number of species with a great diversity of ecologies, reproductive strategies, and developmental pathways. More recently, an expressed sequence tag (EST) study was done to identify the Acps of D. mojavensis (Wagstaff and Begun 2005b), a species of the repleta group. This group belongs in a different subgenus of Drosophila than the other species studied thus far (Throckmorton 1975). The repleta group represents one of the biggest radiations in the genus Drosophila (Durando et al. 2000). The species in this group have a very different reproductive biology as compared to the melanogaster group flies. Higher remating rates, frequent formation of an insemination reaction that prevents remating for a few hours, and high levels of seminal fluid absorption by the female are some of these differences (Markow and Ankney 1988; Pitnick et al. 1997;Knowles andMarkow 2001). One question that arises is whether the Acp complement can account for these differences. Wagstaff and Begun (2005b) results confirm some of the previous findings in other Drosophila species, such as a high evolutionary rate of Acps as compared to non-Acp genes (in this case, testis expressed genes). Nevertheless, since accessory glands were not dissected separately in that study, it was not possible to make a thorough comparison of the D. mojavensis Acp complement with that of other Drosophila species.

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Orthology, Function and Evolution of Accessory Gland Proteins in the Drosophila Repleta Group
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