Evolution of reproductive morphology among recently diverged taxa in the Drosophila mojavensis species cluster

Division of Biological Sciences, Section of Cell and Developmental Biology, University of California San Diego, La Jolla, California 92093.
Ecology and Evolution (Impact Factor: 2.32). 02/2012; 2(2):397-408. DOI: 10.1002/ece3.93
Source: PubMed


The morphological evolution of sexual traits informs studies of speciation due to the potential role of these characters in reproductive isolation. In the current study, we quantified and compared genitalic variation within the Drosophila mojavensis species cluster to infer the mode of evolution of the male aedeagus. This system is ideal for such studies due to the opportunity to test and compare levels of variation along a divergence continuum at various taxonomic levels within the group. Shape variation was quantified using elliptic Fourier descriptors and compared among the four D. mojavensis host races, and between D. mojavensis and its sister species Drosophila arizonae. Aedeagus shape was diagnostic for D. arizonae, and among three of the four D. mojavensis subspecies. In each of these cases, there was less variation within subspecies than among subspecies, which is consistent with the pattern predicted if genitalia are evolving according to a punctuated change model, and are involved with mate recognition. However, aedeagus shape in Drosophila mojavensis sonorensis was highly variable and broadly overlapping with the other three subspecies, suggesting aedeagus evolution in this subspecies is more complex and subject to additional evolutionary factors. These results are interpreted and discussed in the context of selection on mate recognition systems and the potential for failed copulation.

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Available from: Maxi Polihronakis Richmond
    • "Genital adaptations that confer upon males a competitive advantage may consequently reduce female fitness (Arnqvist & Rowe, 2005) and lead to sexually antagonistic coevolution between male and female morphologies (Arnqvist & Rowe, 2002a,2002b; Rönn et al., 2007; Tatarnic & Cassis, 2010). Although genital characters are ubiquitous taxonomic tools and used heavily in constructing phylogenetic relationships, the independent mapping of genital traits onto molecular phylogenies is less common, but has been highlighted in several recent studies (Richmond et al., 2012; Wojcieszek & Simmons, 2012; Yassin & Orgogozo, 2013). Mapping divergent genital morphologies onto molecular phylogenies can allow ancestral states to be reconstructed, and allow one to assess the likelihood of independent or convergent evolution of specific genital characters (Barmina & Kopp, 2007; Scharer et al., 2011). "
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    ABSTRACT: Male genitalia are among the most rapidly evolving and divergent morphological structures and sexual selection is known to drive this phenomenon in many taxa. Because of their diversity, even within a single genus, genital characters are frequently used to infer relationships among closely-related species. Moths within the genus Izatha (Xyloryctidae) are ideal candidates for investigating the phylogenetic patterns of genital evolution as they display great variation in male genital structure and complexity. We determined the evolutionary relationships among 31 species of Izatha by constructing a molecular phylogeny of the genus based on the mitochondrial cytochrome oxidase subunit I gene and the isocitrate dehydrogenase and carbamoylphosphate synthase domain protein nuclear genes. This allowed estimations of ancestral male genital character states and patterns of male genital diversification using maximum-likelihood models. The genus is divided into two well-supported clades and two poorly supported clades at the root of the phylogeny with incomplete phylogenetic resolution within two species groups, likely due to rapid speciation. Izatha display a number of apomorphic phallic traits including cornuti (sclerotized spines) which are either discharged into the female during copulation (deciduous cornuti) or fixed to the male phallus (compound and fish-hook cornuti). Within the genus, there is a reduction of secondary genital characters - the uncus and gnathos - but an elaboration of another grasping structure, the juxta; the potential origin and functionality of these male genital traits are discussed. Overall, some male genital characters provided a good indication of species relationships; however, several parts of the complex male genitalia of Izatha show evidence of homoplasy and convergence highlighting the problems of using these traits in determining species relationships. Additionally, this convergence has highlighted that complex genital structures may evolve repeatedly and independently within a lineage.
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    • "Thorax length is a significant life history trait, given its correlation with other characteristics such as flight performance, stress resistance, ovariole number (which is correlated with lifetime fecundity) and mating success (Markow and Ricker 1992; Azevedo et al. 1998; Hoffmann et al. 2001; Mangan 1978). Several morphological and pigmentation differences have been identified across all four host races, most notably divergence in features of the male genitalia such as the shape of the aedeagus (Richmond et al. 2012; Pfeiler et al. 2009). Overall, D. mojavensis is highly resistant to water stress relative to other Drosophila (Gibbs et al. 2003; Gibbs and Matzkin 2001; Matzkin et al. 2009), but yet significant differences in desiccation resistance exist between Catalina, Baja California and Sonora populations (Rajpurohit et al. 2013; Matzkin et al. 2007). "
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    ABSTRACT: Advances in next-generation sequencing technologies have liberated our dependency on model laboratory species for answering genomic and transcriptomic level questions. These new techniques have dramatically expanded our breadth of study organisms and have allowed the analysis of species from diverse ecological environments. One such species is the cactophilic Drosophila mojavensis that inhabits the deserts of western North America. These insects feed and develop in the necrotic cacti, feeding largely on the microflora of the necrotic plant tissues. Drosophila mojavensis is composed of four geographically and ecologically separated populations. Each population (Baja California peninsula, mainland Sonoran Desert, Mojave Desert and Santa Catalina Island) utilizes the necrotic tissues of distinct cactus species. The differences in the nutritional and chemical composition of the necroses include a set of toxic compounds to which resident population must adapt. These ecological differences have facilitated many of the life history, behavior, physiological and genetic differences between the cactus host populations. Genomic resources have allowed investigators to examine the genomic and transcriptional level changes associated with the local adaptation of the four D. mojavensis populations, thereby providing further understanding of the genetic mechanism of adaptation and its role in the divergence of ecologically distinct populations.
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    • "Studies involving members of the repleta group have shown that females have high FRRs (Markow 1996; Bundgaard & Barker 2000; Good et al. 2006) and extremely rapid evolutionary rates of some reproductive tract proteins (Wagstaff & Begun 2005; Kelleher et al. 2011). In addition, it has been established that male genital morphology exhibits rapid adaptive evolution in Drosophila mojavensis (Richmond et al. 2012) and Drosophila buzzatii (Soto et al. 2013). Recently, Hurtado & Hasson (2013) found that female latency to remating is 14 times shorter in D. buzzatii than in D. koepferae, which suggests that female remating frequency and SC opportunities are quite higher in D. buzzatii. "
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    ABSTRACT: Sperm competition (SC) is a major component of sexual selection that enhances intra- and intersexual conflicts and may trigger rapid adaptive evolution of sexual characters. The actual role of SC on rapid evolution, however, is poorly understood. Besides, the relative contribution of distinctive features of the mating system to among species variation in the strength of SC remains unclear. Here, we assessed the strength of SC and mating system factors that may account for it in the closely related species Drosophila buzzatii and Drosophila koepferae. Our analyses reveal higher incidence of multiple paternity and SC risk in D. buzzatii wild-inseminated females. The estimated number of fathers per brood was 3.57 in D. buzzatii and 1.95 in D. koepferae. In turn, the expected proportion of females inseminated by more than one male was 0.89 in D. buzzatii and 0.58 in D. koepferae. Laboratory experiments show that this pattern may be accounted for by the faster rate of stored sperm usage observed in D. koepferae and by the greater female remating rate exhibited by D. buzzatii. We also found that the male reproductive cost of SC is also higher in D. buzzatii. After a female mated with a second male, first-mating male fertility was reduced by 71.4% in D. buzzatii and only 33.3% in D. koepferae. Therefore, we may conclude that postmating sexual selection via SC is a stronger evolutionary force in D. buzzatii than in its sibling.
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