Variation In Effective Population Size Research Articles

Drift drives the evolution of chromosome number II: The impact of range size on genome evolution in Carnivora.

Chromosome number is a fundamental genomic trait that is often the first recorded characteristic of a genome. Across large clades, a common pattern emerges: many or even most lineages exhibit relative stasis, while a handful of lineages or species exhibit striking variation. Despite recent developments in comparative methods, most of this heterogeneity is still poorly understood. It is essential to understand why some lineages have rapid rates of chromosome number evolution, as it can impact a variety of other traits. Previous research suggests that biased female meiotic drive may shape rates of karyotype evolution in some mammals. However, Carnivora exhibits variation that this female meiotic drive model cannot explain. We hypothesize that variation in effective population size may underlie rate variation in Carnivora. To test this hypothesis, we estimated rates of fusions and fissions while accounting for range size, which we use as a proxy for effective population size. We reason fusions and fissions are deleterious or underdominant and that only in lineages with small range sizes will these changes be able to fix due to genetic drift. In this study, we find that the rates of fusions and fissions are elevated in taxa with small range sizes relative to those with large range sizes. Based on these findings, we conclude that 1) naturally occurring structural mutations that change chromosome number are underdominant or mildly deleterious, and 2) when population sizes are small, structural rearrangements may play an important role in speciation and reduction in gene flow among populations.

Genomic diversity landscapes in outcrossing and selfing Caenorhabditis nematodes.

Caenorhabditis nematodes form an excellent model for studying how the mode of reproduction affects genetic diversity, as some species reproduce via outcrossing whereas others can self-fertilize. Currently, chromosome-level patterns of diversity and recombination are only available for self-reproducing Caenorhabditis, making the generality of genomic patterns across the genus unclear given the profound potential influence of reproductive mode. Here we present a whole-genome diversity landscape, coupled with a new genetic map, for the outcrossing nematode C. remanei. We demonstrate that the genomic distribution of recombination in C. remanei, like the model nematode C. elegans, shows high recombination rates on chromosome arms and low rates toward the central regions. Patterns of genetic variation across the genome are also similar between these species, but differ dramatically in scale, being tenfold greater for C. remanei. Historical reconstructions of variation in effective population size over the past million generations echo this difference in polymorphism. Evolutionary simulations demonstrate how selection, recombination, mutation, and selfing shape variation along the genome, and that multiple drivers can produce patterns similar to those observed in natural populations. The results illustrate how genome organization and selection play a crucial role in shaping the genomic pattern of diversity whereas demographic processes scale the level of diversity across the genome as a whole.

Reconstructing the History of Variation in Effective Population Size along Phylogenies.

The nearly neutral theory predicts specific relations between effective population size (Ne) and patterns of divergence and polymorphism, which depend on the shape of the distribution of fitness effects (DFE) of new mutations. However, testing these relations is not straightforward, owing to the difficulty in estimating Ne. Here, we introduce an integrative framework allowing for an explicit reconstruction of the phylogenetic history of Ne, thus leading to a quantitative test of the nearly neutral theory and an estimation of the allometric scaling of the ratios of nonsynonymous over synonymous polymorphism () and divergence (dN/dS) with respect to Ne. As an illustration, we applied our method to primates, for which the nearly neutral predictions were mostly verified. Under a purely nearly neutral model with a constant DFE across species, we find that the variation in and dN/dS as a function of Ne is too large to be compatible with current estimates of the DFE based on site frequency spectra. The reconstructed history of Ne shows a 10-fold variation across primates. The mutation rate per generation u, also reconstructed over the tree by the method, varies over a 3-fold range and is negatively correlated with Ne. As a result of these opposing trends for Ne and u, variation in πS is intermediate, primarily driven by Ne but substantially influenced by u. Altogether, our integrative framework provides a quantitative assessment of the role of Ne and u in modulating patterns of genetic variation, while giving a synthetic picture of their history over the clade.

Expansion history and environmental suitability shape effective population size in a plant invasion.

The margins of an expanding range are predicted to be challenging environments for adaptation. Marginal populations should often experience low effective population sizes (Ne ) where genetic drift is high due to demographic expansion and/or census population size is low due to unfavourable environmental conditions. Nevertheless, invasive species demonstrate increasing evidence of rapid evolution and potential adaptation to novel environments encountered during colonization, calling into question whether significant reductions in Ne are realized during range expansions in nature. Here we report one of the first empirical tests of the joint effects of expansion dynamics and environment on effective population size variation during invasive range expansion. We estimate contemporary values of Ne using rates of linkage disequilibrium among genome-wide markers within introduced populations of the highly invasive plant Centaurea solstitialis (yellow starthistle) in North America (California, USA), and within native Eurasian populations. As predicted, we find that Ne within the invaded range is positively correlated with both expansion history (time since founding) and habitat quality (abiotic climate). History and climate had independent additive effects with similar effect sizes, indicating an important role for both factors in this invasion. These results support theoretical expectations for the population genetics of range expansion, though whether these processes can ultimately arrest the spread of an invasive species remains an unanswered question.

Demographic Expansion and Contraction in a Neotropical Fish during the Late Pleistocene-Holocene

Demographic changes during the late Pleistocene-Holocene left signatures in the DNA of contemporary populations. These signatures reveal demographic phenomena like the increase or decrease in effective population size. In this paper we searched for signatures of demographic change in the DNA of the Neotropical freshwater fish Poecilia vivipara. Also, we investigated whether demographic changes are correlated with palaeoclimatic events of the late Pleistocene-Holocene, in particular, if changes in effective population size are correlated with expansion and contraction of available habitats, induced by global ice-volume changes and sea-level fluctuations. We used Bayesian Skyline Plot (BSP) analysis with sequences from the mitochondrial gene cytochrome b to estimate the ancestral demography of the Neotropical freshwater fish P. vivipara. To test the assumptions of neutrality and absence of population structure we used Tajima’s D and Spatial Analysis of Molecular Variance (SAMOVA), respectively. Effective population size of P. vivipara remained stable until 75,000 years ago, increased by 10-fold reaching a maximum at approximately 25,000 years ago, then suddenly declined at the Pleistocene-Holocene boundary. Variation in effective population size in P. vivipara correlates with expansion and contraction of habitats induced by sea-level fluctuations, caused by the advance and retreat of ice sheets during the Last Glacial Maximum (LGM).

Genetic diversity of the African malaria vector Anopheles gambiae.

The sustainability of malaria control in Africa is threatened by the rise of insecticide resistance in Anopheles mosquitoes, which transmit the disease. To gain a deeper understanding of how mosquito populations are evolving, here we sequenced the genomes of 765 specimens of Anopheles gambiae and Anopheles coluzzii sampled from 15 locations across Africa, and identified over 50 million single nucleotide polymorphisms within the accessible genome. These data revealed complex population structure and patterns of gene flow, with evidence of ancient expansions, recent bottlenecks, and local variation in effective population size. Strong signals of recent selection were observed in insecticide-resistance genes, with several sweeps spreading over large geographical distances and between species. The design of new tools for mosquito control using gene-drive systems will need to take account of high levels of genetic diversity in natural mosquito populations.

Modeling the Multiple Facets of Speciation-with-Gene-Flow toward Inferring the Divergence History of Lake Whitefish Species Pairs (Coregonus clupeaformis).

Parallel divergence across replicated species pairs occurring in similar environmental contrasts may arise through distinct evolutionary scenarios. Deciphering whether such parallelism actually reflects repeated parallel divergence driven by divergent selection or a single divergence event with subsequent gene flow needs to be ascertained. Reconstructing historical gene flow is therefore of fundamental interest to understand how demography and selection jointly shaped genomic divergence during speciation. Here, we use an extended modeling framework to explore the multiple facets of speciation-with-gene-flow with demo-genetic divergence models that capture both temporal and genomic variation in effective population size and migration rate. We investigate the divergence history of replicate sympatric species pairs of Lake Whitefish (normal benthic and dwarf limnetic) characterized by variable degrees of ecological divergence and reproductive isolation. Genome-wide SNPs were used to document the extent of genetic differentiation in each species pair, and 26 divergence models were fitted and compared with the unfolded joint allele frequency spectrum of each pair. We found evidence that a recent (circa 3,000–4,000 generations) asymmetrical secondary contact between expanding postglacial populations has accompanied Whitefish diversification. Our results suggest that heterogeneous genomic differentiation has emerged through the combined effects of linked selection generating variable rates of lineage sorting across the genome during geographical isolation, and heterogeneous introgression eroding divergence at different rates across the genome upon secondary contact. This study thus provides a new retrospective insight into the historical demographic and selective processes that shaped a continuum of divergence associated with ecological speciation.

Population Genomics of Daphnia pulex.

Using data from 83 isolates from a single population, the population genomics of the microcrustacean Daphnia pulex are described and compared to current knowledge for the only other well-studied invertebrate, Drosophila melanogaster These two species are quite similar with respect to effective population sizes and mutation rates, although some features of recombination appear to be different, with linkage disequilibrium being elevated at short ([Formula: see text] bp) distances in D. melanogaster and at long distances in D. pulex The study population adheres closely to the expectations under Hardy-Weinberg equilibrium, and reflects a past population history of no more than a twofold range of variation in effective population size. Fourfold redundant silent sites and a restricted region of intronic sites appear to evolve in a nearly neutral fashion, providing a powerful tool for population genetic analyses. Amino acid replacement sites are predominantly under strong purifying selection, as are a large fraction of sites in UTRs and intergenic regions, but the majority of SNPs at such sites that rise to frequencies [Formula: see text] appear to evolve in a nearly neutral fashion. All forms of genomic sites (including replacement sites within codons, and intergenic and UTR regions) appear to be experiencing an [Formula: see text] higher level of selection scaled to the power of drift in D. melanogaster, but this may in part be a consequence of recent demographic changes. These results establish D. pulex as an excellent system for future work on the evolutionary genomics of natural populations.

Assessing the genetic diversity of the mangrove oyster Crassostrea rhizophorae (Bivalvia, Ostreidae) by microsatellite markers in southeastern Brazil

Oysters of the genus Crassostrea are an economically important resource occurring along the Brazilian coast, mainly in estuarine regions. Inter- and intra-population genetic diversity is essential for monitoring long-term genetic changes and for sustainable use of this bivalve by coastal fishing communities. Microsatellite markers were used to evaluate the genetic diversity of natural populations of the mangrove oyster Crassostrea rhizophorae in southeastern Brazil. Samples of 150 oysters from four areas were analyzed. Microsatellite loci were obtained from an enriched microsatellite library. The genetic structure was evaluated using an index of genetic differentiation described previously. The effective population size and rate of gene flow were estimated through a maximum likelihood coalescent approach using Migrate. The mean number of alleles ranged from 10 to 21 and the expected heterozygosity from 0.89 to 0.91. Evidence of a possible bottleneck effect under three mutational models was found. The Dest index indicated low to moderate differentiation among sample locales. Coalescent analysis showed variation in effective population size and asymmetry in the gene flow among samples. Levels of genetic variability and differentiation found among C. rhizophorae populated banks have important implications for the sustainable harvest, cultivation and conservation of this marine resource in the studied area.

Reconstructing the phylogenetic history of long-term effective population size and life-history traits using patterns of amino acid replacement in mitochondrial genomes of mammals and birds.

The nearly neutral theory, which proposes that most mutations are deleterious or close to neutral, predicts that the ratio of nonsynonymous over synonymous substitution rates (dN/dS), and potentially also the ratio of radical over conservative amino acid replacement rates (Kr/Kc), are negatively correlated with effective population size. Previous empirical tests, using life-history traits (LHT) such as body-size or generation-time as proxies for population size, have been consistent with these predictions. This suggests that large-scale phylogenetic reconstructions of dN/dS or Kr/Kc might reveal interesting macroevolutionary patterns in the variation in effective population size among lineages. In this work, we further develop an integrative probabilistic framework for phylogenetic covariance analysis introduced previously, so as to estimate the correlation patterns between dN/dS, Kr/Kc, and three LHT, in mitochondrial genomes of birds and mammals. Kr/Kc displays stronger and more stable correlations with LHT than does dN/dS, which we interpret as a greater robustness of Kr/Kc, compared with dN/dS, the latter being confounded by the high saturation of the synonymous substitution rate in mitochondrial genomes. The correlation of Kr/Kc with LHT was robust when controlling for the potentially confounding effects of nucleotide compositional variation between taxa. The positive correlation of the mitochondrial Kr/Kc with LHT is compatible with previous reports, and with a nearly neutral interpretation, although alternative explanations are also possible. The Kr/Kc model was finally used for reconstructing life-history evolution in birds and mammals. This analysis suggests a fairly large-bodied ancestor in both groups. In birds, life-history evolution seems to have occurred mainly through size reduction in Neoavian birds, whereas in placental mammals, body mass evolution shows disparate trends across subclades. Altogether, our work represents a further step toward a more comprehensive phylogenetic reconstruction of the evolution of life-history and of the population-genetics environment.

Theoretical limits to the correlation between pelagic larval duration and population genetic structure

Increasing dispersal duration should result in increasing dispersal distance, facilitating higher gene flow among populations. As such, it has long been predicted that genetic structure (e.g. F(ST) ) among populations of marine species should be strongly correlated with pelagic larval duration (PLD). However, previous studies have repeatedly shown a surprisingly poor correspondence. This result has been frequently interpreted as evidence for larval behaviours or physical oceanographic processes that result in larvae failing to reach their dispersal potential, or error inherent in estimating PLD and F(ST) . This study employed a computer modelling approach to explore the impacts of various uncertainties on the correlation between measures of genetic differentiation such as F(ST) and PLD. Results indicate that variation resulting from PLD estimation error had minor impacts on the correlation between genetic structure and PLD. However, variation in effective population size between species, errors in F(ST) estimation and non-equilibrium F(ST) values all had major impacts, resulting in dramatically weaker correlations between PLD and F(ST) . These results suggest that poor correlations between PLD and F(ST) may result from variation and uncertainty in the terms associated with the calculation of F(ST) values. As such, PLD may be a much stronger determinant of realized larval dispersal than suggested by the weak-to-moderate correlations between PLD and F(ST) reported in empirical studies.

GEOGRAPHICAL VARIATION IN THE RATE OF EVOLUTION: EFFECT OF AVAILABLE ENERGY OR FLUCTUATING ENVIRONMENT?

In a recent paper, Wright et al. (2003) argue for the hypothesis that greater biologically available energy elevates the rate of molecular evolution. However, their results are also consistent with alternative hypotheses that invoke either environmentally driven variation in effective population sizes, or natural selection, or both. The available energy gradient cited by Wright et al. is linearly correlated with temperature fluctuations, and the observed rate heterogeneity could be a consequence of this environmental variability. The distribution of phylogenetic branch lengths alone is insufficient to distinguish between the hypotheses, and complementary approaches are suggested.

Microsatellite variation in natural Drosophila melanogaster populations from New South Wales (Australia) and Tasmania.

Microsatellite variation was studied at 48 microsatellite loci in 10 Drosophila melanogaster populations to investigate the population structure on the Australian east coast. Low, but statistically significant population differentiation was observed among most populations. The populations on the Australian mainland did not show evidence for isolation by distance. We conclude that the population structure of D. melanogaster on the Australian mainland is probably the result of a shared history (recent colonization). The observed differences between local D. melanogaster populations probably reflect variation in effective population sizes rather than patterns of gene flow. Two populations from Tasmania were more differentiated from the Australian mainland than a population from Israel, raising the question whether they are derived from the Australian mainland or colonized from a different source population.

Within population variation in the demography of Speyeria mormonia (Lepidoptera: Nymphalidae)

The adult demography of a population of Speyeria mormonia (Lepidoptera: Nymphalidae) near Gothic, Colorado USA was studied for four years. Values of demographic parameters, including survival, dispersal and sex ratio, varied yearly, without major changes in density. Shift in sex ratio with constant population numbers entails variation in effective population size among years. Flight period, catchability, relationship between body size and eclosion date, and significance of correlation between weather and daily survival rates differed between the sexes. Sexual dimorphism in correlation of wheather with survival rate may partially explain the lack of yearly variation in total population size. There was no significant sexual dimorphism in large scale habitat use, or in dispersal, except in 1982.The demography of this insect is compared to that of related species of Argynnis and heliconiines, from the old world temperate zone and new world tropics, respectively. While some differences are observed which can be ascribed to differences in length of the growing season, many patterns are similar. This implies conservation of demographic traits, even across broad habitat and geographic areas.

MACRO- AND MICROGEOGRAPHIC STRUCTURE OF A SPATIALLY SUBDIVIDED BEETLE SPECIES IN NATURE.

Spatial subdivision of species can affect their population structure by allowing processes such as limited dispersal, spatial heterogeneity in selective pressures, small population sizes, and random events to operate. By studying species restricted to islands or "island" habitats, one can attempt to determine which of these factors have affected the current structure of the population. Collops georgianus (Coleoptera: Melyridae), a beetle species endemic to the "island" habitat of granitic rock outcrops, was chosen to see how its spatially subdivided distribution has affected its genetic structure. Its genetic structure was examined on both a macrogeographic and a microgeographic level using protein electrophoresis. Macrogeographically, 12 populations throughout its range were sampled. The discontinuous distribution of outcrops, and thus populations, throughout its range, has determined the connectivity of the populations. Significant variation in allele frequencies and substructuring (FST = 0.192) was found throughout the range, but there was no spatial autocorrelation. Microgeographically, in the central part of the range, where outcrops are denser and more continuously distributed in space, there was evidence of isolation by distance. Very little variation in allele frequencies was found, but a low but significant level of substructuring occurred among the populations. Comparison of disjunct and continuous populations microgeographically revealed no effect of disjunct distributions, although a significant effect of distance was detected. Effective population size variation among populations and between years, compounded with the effects of local extinctions, suggest that random processes such as drift and founder effects are important determinants of the population's genetic structure.