Effects of selection and drift on genital morphology and accessory gland proteins in natural Drosophila melanogaster populations
Zusammenfassung der Projektergebnisse
In insects such as Drosophila, male genitalia and accessory gland proteins (Acp’s) show strikingly rapid and divergent evolution. Sexual selection rather than neutrality has been invoked to explain the patterns. However, the comparative evidence for this hypothesis remains scarce and largely restricted to inter-specific analyses focussing on long-term evolutionary changes. This project represented an explicit assessment of the roles of drift and selection in shaping the evolution of genital morphology and seminal fluid proteins by comparing multiple natural populations of Drosophila melanogaster. My main motivation was to obtain a better understanding of the evolutionary dynamics of male reproductive traits in general and the potential role of sexual selection leading to divergence before reproductive isolation has evolved. For the investigation of the posterior lobe of the male genital arch –a derived structure specific to D. melanogaster group species, I raised 215 iso-female lines originating from 23 geographically distinct populations over four continents under standardized conditions. I also scored sex comb teeth number, as well as wing morphology and tibia length. The application of two developmental temperatures further provided valuable information on the phenotypic plasticity and scaling relationships of the focal traits. The core results and their implications are as follows: Firstly, although populations were found to harbour substantial standing genetic variation for all study traits (indicating a great potential for evolutionary change if exposed to selection), shape differences in genital morphology were smaller than expected under neutrality, and largely corresponded to that of wing vein positioning. The low differentiation in genital shape stands in striking contrast to the high divergence between species, indicating discordant rates of evolution. i.e., an actual selective pressure distinct from that in the past. Secondly, in contrast to shape, genital size revealed a strong phylogenetic signal with derived cosmopolitan European and Asian flies developing larger genitalia compared to the ancestral sub-Saharan African populations. Drift alone can to a large extent explain this pattern. This interpretation also applies to sex comb teeth number, a trait supposed to evolve under sexual selection in Drosophila. Finally, the studied traits greatly varied in plasticity with ancestral sub-Saharan flies being phenotypically more canalized than the derived, cosmopolitan Asian and European flies. This finding indicates that a substantial fraction of the morphological diversification related to the out-of-Africa range expansion in D. melanogaster is accompanied by the evolution of phenotypic plasticity, and further implicates that the hot tropical temperature per se does not strongly select against phenotypic plasticity once it has evolved. Interestingly, despite the large variation in plasticity of the different traits, allometric scaling relationships appear to be highly conserved across continents and temperatures. The population genetic analysis of the Acp’s was performed using whole genome sequences of eight D. melanogaster populations including two from sub-Saharan Africa, one from Central America and five from Europe. Each population was sequenced using pooled DNA samples of multiple individuals with an Illumina Genome Analyzer IIx and subsequently mapped against the FlyBase D. melanogaster reference genome sequence (release r5.38). The sequences of more than 100 Acps and a comparable set of reference genes were then extracted from the genomes and analyzed. Reference genes of similar size and with no established function in reproduction were selected in the flanking genomic region of the Acp’s to account for differences in chromosomal location and recombination. The analyses lead me to the following main conclusions. Firstly, in contrast to previous inter-species analyses, which documented that the male seminal fluid transferred to female Drosophila during mating is enriched for genes that diverge rapidly and often show signatures of positive selection, my population-based approach did not reveal that Acp’s are more differentiated than other genes within D. melanogaster. This observation does not preclude spatially divergent selection on some loci, but rather means that its magnitude does not systematically vary between the different classes of genes. Secondly, balancing or frequency dependent selection has been invoked to explain the high degree of amino-acid replacement polymorphisms in seminal fluid proteins. In agreement with the literature, I found that Acp’s are on average more polymorphic than other genes at replacement sites, This is not the case for silent sites. In addition, my data revealed that the allele frequency spectrum of non-synonymous substitutions in the Acp’s is significantly shifted towards fewer rare alleles, which is indicated by less negative Tajima’s D values. Several Acps even showed a positive Tajima’s D above 1, suggestive of balancing selection. Information on the haplotype structure will help to clarify this issue. Finally, although my study provided a number of candidate genes that might be under selection, much of the sequence variation in the Acp’s can be explained by neutrality, such as the high level of amino-acid replacement polymorphisms and also the shift in the allele spectrum of many Acp’s towards neutral expectations.
Projektbezogene Publikationen (Auswahl)
- 2010. ‘Latitudinal variation and temperature-dependent plasticity of a polymorphic sperm storage organ’. 103th annual meeting of the German Zoological Society (DZG), Hamburg, Germany; Biology10 meeting of the Swiss Zoological Society, Neuchatel, Switzerland
- A microsatellite linkage map for Drosophila montana shows large variation in recombination rates, and a courtship song trait maps to an area of low recombination. Journal of Evolutionary Biology 23: 518-527, 2010
Schäfer MA, Routtu J, Vieira J, Hoikkala A, Ritchie MG and Schlötterer C
- 2011. ‘Selection vs drift affecting population genetic variation in genital morphology in Drosophila melanogaster’. 13th Congress of the European Society for Evolutionary Biology, Tübingen, Germany
- High temperatures reveal cryptic genetic variation in a polymorphic female sperm storage organ. Evolution 65: 2830-2842, 2011
Berger D, Bauerfeind, SS, Blanckenhorn WU and Schäfer MA
- Multiple quantitative trait loci influence intra-specific variation in genital morphology between phylogenetically distinct lines of Drosophila montana. Journal of Evolutionary Biology 24: 1879-1886, 2011
Schäfer MA, Routtu J, Vieira J, Hoikkala A, Ritchie MG and Schlötterer C
