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

Practice-oriented controversies and borrowed epistemic credibility in current evolutionary biology: phylogeography as a case study

Although there is increasing recognition that theory and practice in science are intimately intertwined, philosophy of science perspectives on scientific controversies have been historically focused on theory rather than practice. As a step in the construction of frameworks for understanding controversies linked to scientific practices, here we introduce the notion of borrowed epistemic credibility (BEC), to describe the situation in which scientists, in order to garner support for their own stances, exploit similarities between tenets in their own field and accepted statements or positions properly developed within other areas of expertise. We illustrate the scope of application of our proposal with the analysis of a heavily methods-grounded, recent controversy in phylogeography, a biological subdiscipline concerned with the study of the historical causes of biogeographical variation through population genetics- and phylogenetics-based computer analyses of diversity in DNA sequences, both within species and between closely related taxa. Toward this end, we briefly summarize the arguments proposed by selected authors representing each side of the controversy: the ‘nested clade analysis’ school versus the ‘statistical phylogeography’ orientation. We claim that whereas both phylogeographic ‘research styles’ borrow epistemic credibility from sources such as formal logic, the familiarity of results from other scientific areas, the authority of prominent scientists, or the presumed superiority of quantitative vs. verbal reasoning, ‘theory’ plays essentially no role as a foundation of the controversy. Besides underscoring the importance of strictly methodological and other non-theoretical aspects of controversies in current evolutionary biology, our analysis suggests a perspective with potential usefulness for the re-examination of more general philosophy of biology issues, such as the nature of historical inference, rationality, justification, and objectivity

Evidence for convergent nucleotide evolution and high allelic turnover rates at the complementary sex determiner (csd) gene of western and Asian honey bees

Our understanding of the impact of recombination, mutation, genetic drift and selection on the evolution of a single gene is still limited. Here we investigate the impact of all of these evolutionary forces at the complementary sex determiner (csd) gene which evolves under a balancing mode of selection. Females are heterozygous at the csd gene and males are hemizygous; diploid males are lethal and occur when csd is homozygous. Rare alleles thus have a selective advantage, are seldom lost by the effect of genetic drift and are maintained over extended periods of time when compared to neutral polymorphisms. Here, we report on the analysis of 17, 19 and 15 csd alleles of Apis cerana, Apis dorsata and Apis mellifera honey bees respectively. We observed great heterogeneity of synonymous (pi S) and nonsynonymous (pi N) polymorphisms across the gene, with a consistent peak in exon 6 and 7. We propose that exons 6 and 7 encode the potential specifying domain (csd-PSD) which has accumulated elevated nucleotide polymorphisms over time by balancing selection. We observed no direct evidence that balancing selection favors the accumulation of nonsynonymous changes at csd-PSD (pi N/pi S ratios are all < 1, ranging from 0.6 to 0.95). We observed an excess of shared nonsynonymous changes, which suggests that strong evolutionary constraints are operating at csd-PSD resulting in the independent accumulation of the same nonsynonymous changes in different alleles across species (convergent evolution). Analysis of a csd-PSD genealogy revealed relatively short average coalescence times (~6 million years), low average synonymous nucleotide diversity (pi S < 0.09) and a lack of trans-specific alleles which substantially contrasts with previously analyzed loci under strong balancing selection. We excluded the possibility of a burst of diversification after population bottlenecking and intragenic recombination as explanatory factors, leaving high turn-over rates as the explanation for this observation. By comparing observed allele richness and average coalescence times with a simplified model of csd-coalescence, we found that small long term population sizes (i.e. Ne <104), but not high mutation rates, can explain short maintenance times, implicating a strong impact of genetic drift on the molecular evolution of highly social honey bees

Spotlight on islands.On the origin and diversification of an ancient lineage of the Italian wall lizard Podarcis siculus in the western Pontine Islands

Groups of proximate continental islands may conceal more tangled phylogeographic patterns than oceanic archipelagos as a consequence of repeated sea level changes, which allow populations to experience gene flow during periods of low sea level stands and isolation by vicariant mechanisms during periods of high sea level stands. Here, we describe for the first time an ancient and diverging lineage of the Italian wall lizard Podarcis siculus from the western Pontine Islands. We used nuclear and mitochondrial DNA sequences of 156 individuals with the aim of unraveling their phylogenetic position, while microsatellite loci were used to test several a priori insular biogeographic models of migration with empirical data. Our results suggest that the western Pontine populations colonized the islands early during their Pliocene volcanic formation, while populations from the eastern Pontine Islands seem to have been introduced recently. The inter-island genetic makeup indicates an important role of historical migration, probably due to glacial land bridges connecting islands followed by a recent vicariant mechanism of isolation. Moreover, the most supported migration model predicted higher gene flow among islands which are geographically arranged in parallel. Considering the threatened status of small insular endemic populations, we suggest this new evolutionarily independent unit be given priority in conservation efforts

Inferring Species Trees Directly from Biallelic Genetic Markers: Bypassing Gene Trees in a Full Coalescent Analysis

The multi-species coalescent provides an elegant theoretical framework for estimating species trees and species demographics from genetic markers. Practical applications of the multi-species coalescent model are, however, limited by the need to integrate or sample over all gene trees possible for each genetic marker. Here we describe a polynomial-time algorithm that computes the likelihood of a species tree directly from the markers under a finite-sites model of mutation, effectively integrating over all possible gene trees. The method applies to independent (unlinked) biallelic markers such as well-spaced single nucleotide polymorphisms (SNPs), and we have implemented it in SNAPP, a Markov chain Monte-Carlo sampler for inferring species trees, divergence dates, and population sizes. We report results from simulation experiments and from an analysis of 1997 amplified fragment length polymorphism (AFLP) loci in 69 individuals sampled from six species of {\em Ourisia} (New Zealand native foxglove)

Genome-wide inference of ancestral recombination graphs

The complex correlation structure of a collection of orthologous DNA sequences is uniquely captured by the "ancestral recombination graph" (ARG), a complete record of coalescence and recombination events in the history of the sample. However, existing methods for ARG inference are computationally intensive, highly approximate, or limited to small numbers of sequences, and, as a consequence, explicit ARG inference is rarely used in applied population genomics. Here, we introduce a new algorithm for ARG inference that is efficient enough to apply to dozens of complete mammalian genomes. The key idea of our approach is to sample an ARG of n chromosomes conditional on an ARG of n-1 chromosomes, an operation we call "threading." Using techniques based on hidden Markov models, we can perform this threading operation exactly, up to the assumptions of the sequentially Markov coalescent and a discretization of time. An extension allows for threading of subtrees instead of individual sequences. Repeated application of these threading operations results in highly efficient Markov chain Monte Carlo samplers for ARGs. We have implemented these methods in a computer program called ARGweaver. Experiments with simulated data indicate that ARGweaver converges rapidly to the true posterior distribution and is effective in recovering various features of the ARG for dozens of sequences generated under realistic parameters for human populations. In applications of ARGweaver to 54 human genome sequences from Complete Genomics, we find clear signatures of natural selection, including regions of unusually ancient ancestry associated with balancing selection and reductions in allele age in sites under directional selection. Preliminary results also indicate that our methods can be used to gain insight into complex features of human population structure, even with a noninformative prior distribution.Comment: 88 pages, 7 main figures, 22 supplementary figures. This version contains a substantially expanded genomic data analysi

The era of the ARG: an empiricist's guide to ancestral recombination graphs

In the presence of recombination, the evolutionary relationships between a set of sampled genomes cannot be described by a single genealogical tree. Instead, the genomes are related by a complex, interwoven collection of genealogies formalized in a structure called an ancestral recombination graph (ARG). An ARG extensively encodes the ancestry of the genome(s) and thus is replete with valuable information for addressing diverse questions in evolutionary biology. Despite its potential utility, technological and methodological limitations, along with a lack of approachable literature, have severely restricted awareness and application of ARGs in empirical evolution research. Excitingly, recent progress in ARG reconstruction and simulation have made ARG-based approaches feasible for many questions and systems. In this review, we provide an accessible introduction and exploration of ARGs, survey recent methodological breakthroughs, and describe the potential for ARGs to further existing goals and open avenues of inquiry that were previously inaccessible in evolutionary genomics. Through this discussion, we aim to more widely disseminate the promise of ARGs in evolutionary genomics and encourage the broader development and adoption of ARG-based inference.Comment: 34 pages, 3 figures, 3 table

Genomic Relationships and Speciation Times of Human, Chimpanzee, and Gorilla Inferred from a Coalescent Hidden Markov Model

The genealogical relationship of human, chimpanzee, and gorilla varies along the genome. We develop a hidden Markov model (HMM) that incorporates this variation and relate the model parameters to population genetics quantities such as speciation times and ancestral population sizes. Our HMM is an analytically tractable approximation to the coalescent process with recombination, and in simulations we see no apparent bias in the HMM estimates. We apply the HMM to four autosomal contiguous human–chimp–gorilla–orangutan alignments comprising a total of 1.9 million base pairs. We find a very recent speciation time of human–chimp (4.1 ± 0.4 million years), and fairly large ancestral effective population sizes (65,000 ± 30,000 for the human–chimp ancestor and 45,000 ± 10,000 for the human–chimp–gorilla ancestor). Furthermore, around 50% of the human genome coalesces with chimpanzee after speciation with gorilla. We also consider 250,000 base pairs of X-chromosome alignments and find an effective population size much smaller than 75% of the autosomal effective population sizes. Finally, we find that the rate of transitions between different genealogies correlates well with the region-wide present-day human recombination rate, but does not correlate with the fine-scale recombination rates and recombination hot spots, suggesting that the latter are evolutionarily transient