Signals of demographic expansion in Drosophila virilis

BACKGROUND: The pattern of genetic variation within and among populations of a species is strongly affected by its phylogeographic history. Analyses based on putatively neutral markers provide data from which past events, such as population expansions and colonizations, can be inferred. Drosophila virilis is a cosmopolitan species belonging to the virilis group, where divergence times between different phylads go back to the early Miocene. We analysed mitochondrial DNA sequence variation among 35 Drosophila virilis strains covering the species' range in order to detect demographic events that could be used to understand the present characteristics of the species, as well as its differences from other members of the group. RESULTS: Drosophila virilis showed very low nucleotide diversity with haplotypes distributed in a star-like network, consistent with a recent world-wide exponential expansion possibly associated either with domestication or post-glacial colonization. All analyses point towards a rapid population expansion. Coalescence models support this interpretation. The central haplotype in the network, which could be interpreted as ancestral, is widely distributed and gives no information about the geographical origin of the population expansion. The species showed no geographic structure in the distribution of mitochondrial haplotypes, in contrast to results of a recent microsatellite-based analysis. CONCLUSION: The lack of geographic structure and the star-like topology depicted by the D. virilis haplotypes indicate a pattern of global demographic expansion, probably related to human movements, although this interpretation cannot be distinguished from a selective sweep in the mitochondrial DNA until nuclear sequence data become available. The particular behavioural traits of this species, including weak species-discrimination and intraspecific mate choice exercised by the females, can be understood from this perspective

Not just another genome

Sequence analysis of the Daphnia pulex genome holds some surprises that could not have been anticipated from what was learned so far from other arthropod genomes. It establishes Daphnia as an eco-genetical model organism par excellence

Cold adaptation drives population genomic divergence in the ecological specialist, Drosophila montana

Funding: UK Natural Environment Research Council (Grant Number(s): NE/L501852/1, NE/P000592/1); Academy of Finland (GrantNumber(s): 267244, 268214, 322980), Ella ja Georg Ehrnroothin Säätiö.Detecting signatures of ecological adaptation in comparative genomics is challenging, but analysing population samples with characterised geographic distributions, such as clinal variation, can help identify genes showing covariation with important ecological variation. Here, we analysed patterns of geographic variation in the cold-adapted species Drosophila montana across phenotypes, genotypes and environmental conditions and tested for signatures of cold adaptation in population genomic divergence. We first derived the climatic variables associated with the geographic distribution of 24 populations across two continents to trace the scale of environmental variation experienced by the species, and measured variation in the cold tolerance of the flies of six populations from different geographic contexts. We then performed pooled whole genome sequencing of these six populations, and used Bayesian methods to identify SNPs where genetic differentiation is associated with both climatic variables and the population phenotypic measurements, while controlling for effects of demography and population structure. The top candidate SNPs were enriched on the X and fourth chromosomes, and they also lay near genes implicated in other studies of cold tolerance and population divergence in this species and its close relatives. We conclude that ecological adaptation has contributed to the divergence of D. montana populations throughout the genome and in particular on the X and fourth chromosomes, which also showed highest interpopulation FST. This study demonstrates that ecological selection can drive genomic divergence at different scales, from candidate genes to chromosome-wide effects.Publisher PDFPeer reviewe

Genetic architecture of resistance in Daphnia hosts against two species of host-specific parasites

Understanding the genetic architecture of host resistance is key for understanding the evolution of host–parasite interactions. Evolutionary models often assume simple genetics based on few loci and strong epistasis. It is unknown, however, whether these assumptions apply to natural populations. Using a quantitative trait loci (QTL) approach, we explore the genetic architecture of resistance in the crustacean Daphnia magna to two of its natural parasites: the horizontally transmitted bacterium Pasteuria ramosa and the horizontally and vertically transmitted microsporidium Hamiltosporidium tvaerminnensis. These two systems have become models for studies on the evolution of host–parasite interactions. In the QTL panel used here, Daphnia's resistance to P. ramosa is controlled by a single major QTL (which explains 50% of the observed variation). Resistance to H. tvaerminnensis horizontal infections shows a signature of a quantitative trait based in multiple loci with weak epistatic interactions (together explaining 38% variation). Resistance to H. tvaerminnensis vertical infections, however, shows only one QTL (explaining 13.5% variance) that colocalizes with one of the QTLs for horizontal infections. QTLs for resistance to Pasteuria and Hamiltosporidium do not colocalize. We conclude that the genetics of resistance in D. magna are drastically different for these two parasites. Furthermore, we infer that based on these and earlier results, the mechanisms of coevolution differ strongly for the two host–parasite systems. Only the Pasteuria–Daphnia system is expected to follow the negative frequency-dependent selection (Red Queen) model. How coevolution works in the Hamiltosporidium–Daphnia system remains unclear

Ecological genetics of sediment browsing behaviour in a planktonic crustacean

Zooplankton can display complex habitat selection behaviours that influence the way they interact with their environments. Some species, although primarily pelagic, can exploit sediment-borne particles as a food source or use sediments as a refuge from pelagic predation. However, this strategy may increase the exposure to other risks such as benthic predation and infection from sediment-borne parasite transmission stages. The evolution of habitat selection behaviour in these species is thus expected to be influenced by multiple and possibly contrasting selective forces. Here, we study the browsing behaviour of the water flea Daphnia magna on bottom sediments. First, we demonstrated genetic variation for sediment browsing among D. magna genotypes from natural populations sampled across a broad geographic range. Next, we used an F2 recombinant panel to perform a QTL analysis and identified three regions in the D. magna genome contributing to variation in browsing behaviour. We also analysed the correlation between our data and previously published data on the phototactic behaviour of genotypes from the same F2 panel. Clonal means of the two behavioral traits were not correlated, suggesting that they may evolve independently. Browsing behaviour is likely to be a relevant component of habitat selection in D. magna, and its study may help to incorporate the interactions with the sediment into eco-evolutionary models of this key freshwater species

An SNP-based second-generation genetic map of Daphnia magna and its application to QTL analysis of phenotypic traits

Background: Although Daphnia is increasingly recognized as a model for ecological genomics and biomedical research, there is, as of yet, no high-resolution genetic map for the genus. Such a map would provide an important tool for mapping phenotypes and assembling the genome. Here we estimate the genome size of Daphnia magna and describe the construction of an SNP array based linkage map. We then test the suitability of the map for life history and behavioural trait mapping. The two parent genotypes used to produce the map derived from D. magna populations with and without fish predation, respectively and are therefore expected to show divergent behaviour and life-histories. Results: Using flow cytometry we estimated the genome size of D. magna to be about 238 mb. We developed an SNP array tailored to type SNPs in a D. magna F2 panel and used it to construct a D. magna linkage map, which included 1,324 informative markers. The map produced ten linkage groups ranging from 108.9 to 203.6 cM, with an average distance between markers of 1.13 cM and a total map length of 1,483.6 cM (Kosambi corrected). The physical length per cM is estimated to be 160 kb. Mapping infertility genes, life history traits and behavioural traits on this map revealed several significant QTL peaks and showed a complex pattern of underlying genetics, with different traits showing strongly different genetic architectures. Conclusions: The new linkage map of D. magna constructed here allowed us to characterize genetic differences among parent genotypes from populations with ecological differences. The QTL effect plots are partially consistent with our expectation of local adaptation under contrasting predation regimes. Furthermore, the new genetic map will be an important tool for the Daphnia research community and will contribute to the physical map of the D. magna genome project and the further mapping of phenotypic traits. The clones used to produce the linkage map are maintained in a stock collection and can be used for mapping QTLs of traits that show variance among the F2 clones

Multiple quantitative trait loci influence intra-specific variation in genital morphology between phylogenetically distinct lines of Drosophila montana

The evolution of animal genitalia has gained renewed interest, because of their potential roles during sexual selection and early stages of species formation. Although central to understanding the evolutionary process, knowledge of the genetic basis of natural variation in genital morphology is limited to a very few species. Using an out-bred cross between phylogenetically distinct lines of Drosophila montana, we characterized quantitative trait loci (QTLs) affecting the size and shape of the distiphallus, a prominent part of the male intromittent organ. Our microsatellite-based linkage analysis shows that intra-specific variation of the distiphallus involves several QTLs of largely additive effect and that a highly significant QTL co-localizes with the same inversion where we have earlier localized a large QTL for a sexually selected courtship song trait. The latter indicates that inversions can play an important role in shaping the evolution of rapidly evolving traits with a potential influence on speciation