Demographic history and conservation genomics of caribou (Rangifer tarandus) in Québec

The loss of genetic diversity is a challenge many species are facing, and genomics is a potential tool that can inform and prioritize decision making. Caribou populations have experienced significant recent declines throughout Québec, Canada, and some are considered threatened or endangered. We calculated the ancestral and contemporary patterns of genomic diversity of five caribou populations and applied a comparative framework to assess the interplay between demography and genomic diversity. We calculated a caribou specific mutation rate, μ, by extracting orthologous genes from related ungulates. Whole genome re-sequencing was completed on 67 caribou and genotype likelihoods were estimated. We calculated nucleotide diversity, θπ and estimated the coalescent or ancestral Ne, which ranged from 12,030 to 15,513. When compared to the census size, NC, the endangered Gaspésie Mountain caribou population had the highest Ne:NC ratio which is consistent with recent work suggesting high ancestral Ne:NC is of conservation concern. These ratios were highly correlated with genomic signatures (i.e. Tajima’s D) and explicit demographic model parameters. Values of contemporary Ne, estimated from linkage-disequilibrium, ranged from 11 to 162, with Gaspésie having among the highest contemporary Ne:NC ratio. Importantly, conservation genetics theory would predict this population to be of less concern based on this ratio. Of note, F varied only slightly between populations, and runs of homozygosity were not abundant in the genome. Our study highlights how genomic patterns are nuanced and misleading if viewed only through a contemporary lens; a holistic view should integrate ancestral Ne and Tajima’s D into conservation decisions.

Incorporating rainy season and reproductive phenology into the survival and transition rates of the invasive species Sambucus nigra: An approximation with multi-state models

Although it has been demonstrated that environmental changes within a year can affect the reproduction, survival, and growth of invasive species, these factors have rarely been incorporated into the demographic analysis. Therefore, we applied multi-state demographic models (based on capture–recapture animal methods accounting for imperfect detectability of individuals in natural conditions) to evaluate the effects of reproductive phenology and rainy season on the survival and transition/retrogression rates among stage categories of Sambucus nigra (L)—an invasive tree species, widely distributed in temperate forests of Europe and America. In the Abies religiosa temperate forest, Mexico City, a multi-state demographic model of S. nigra was built using bi-monthly censuses during a year. We selected the best-fitting model according to Akaike’s information criterion (AICc). We determined the response of reproductive phenology of S. nigra to the rainy season for two years through repeatability and phenotypic plasticity indexes. Our results showed that the reproductive phenology of S. nigra has a low repeatability index and a high phenotypic plasticity index. We demonstrated that additive and interactive effects of reproductive phenology and rainy season promote changes in survival and transition/retrogression rates among stage categories. During the rainy season, the survival probability of seedlings and transition probability towards the adult category increased. Therefore, our study represents a significant contribution to the knowledge of the demographic dynamics of invasive species on an intra-annual scale.

Valuation of carbon services produced by wild animals finances conservation

Filling the global biodiversity financing gap will require significant investments from financial markets, which demand credible valuations of ecosystem services and natural capital. However, current valuation approaches discourage investment in conservation because their results cannot be verified using market-determined prices. Here, we bridge the gap between finance and conservation by valuing only wild animals carbon services for which market prices exist. By projecting the future path of carbon service production using a spatially-explicit demographic model, we place a credible value on the carbon-capture services produced by African forest elephants. If elephants were protected, their services would be worth $35.9 billion (24.3-41.2) and store 377 MtC (318-388) across tropical Africa. Our methodology can also place lower bounds on the social cost of nature degradation. Poaching would result in $10-14 billion of lost carbon services. Our methodology enables the integration of animal services into global financial markets with major implications for conservation, local socio-economies, and conservation.

Demographic model and biological adaptation inferred from the genome-wide SNP data reveal tripartite origins of southernmost Chinese Huis

The culturally unique Sanya Hui (SYH) people are regarded as the descendants of ancient Cham people in Central Vietnam (CV) and exhibit a scenario of complex migration and admixture history, who were likely to first migrate from Central and South Asia (CSA) to CV and then to South Hainan and finally assimilated with indigenous populations and resided in the tropical island environments since then. A long-standing hypothesis posits that SYH derives from different genetic and cultural origins, which hypothesizes that SYH people are different from the genetically attested admixture history of northern Hui people possessing major Han-related ancestry and minor western Eurasian ancestry. However, the effect of the cultural admixture from CSA and East Asia (EA) on the genetic admixture of SYH people remains unclear. Here, we reported the first batch of genome-wide SNP data from 94 SYH people from Hainan and comprehensively characterized their genetic structure, origin, and admixture history. Our results found that SYH people were genetically different from the northern Chinese Hui people and harbored a close genomic affinity with indigenous Vietnamese but a distinct relationship with Cham, which confirmed the hypothesis of documented recent historical migration from CV and assimilation with Hainan indigenous people. The fitted admixture models and reconstructed demographic frameworks revealed an additional influx of CSA and EA ancestries during the historical period, consisting of the frequent cultural communication along the Southern Maritime Silk Road and extensive interaction with EA. Analyses focused on natural-selected signatures of SYH people revealed a similar pattern with mainland East Asians, which further confirmed the possibility of admixture-induced biological adaptation of island environments. Generally, three genetically attested ancestries from CV, EA, and CSA in modern SYH people supported their tripartite model of genomic origins.

Population genomics indicate three different modes of divergence and speciation with gene flow in the green-winged teal duck complex

The processes leading to divergence and speciation can differ broadly among taxa with different life histories. We examine these processes in a small clade of ducks with historically uncertain relationships and species limits. The green-winged teal (Anas crecca) complex is a Holarctic species of dabbling duck currently categorized as three subspecies (Anas crecca crecca, A. c. nimia, and A. c. carolinensis) with a close relative, the yellow-billed teal (Anas flavirostris) from South America. We examined divergence and speciation patterns in this group, determining their phylogenetic relationships and the presence and levels of gene flow among lineages using both mitochondrial and genome-wide nuclear DNA obtained from 1,393 ultraconserved element (UCE) loci. Phylogenetic relationships using nuclear DNA among these taxa showed A. c. crecca, A. c. nimia, and A. c. carolinensis clustering together to form one polytomous clade, with A. flavirostris sister to this clade. This relationship can be summarized as (crecca, nimia, carolinensis)(flavirostris). However, whole mitogenomes revealed a different phylogeny: (crecca, nimia)(carolinensis, flavirostris). The best demographic model for key pairwise comparisons supported divergence with gene flow as the probable speciation mechanism in all three contrasts (crecca−nimia, crecca−carolinensis, and carolinensis−flavirostris). Given prior work, gene flow was expected among the Holarctic taxa, but gene flow between North American carolinensis and South American flavirostris (M ~0.1 - 0.4 individuals/generation), albeit low, was not expected. Three geographically oriented modes of divergence are likely involved in the diversification of this complex: heteropatric (crecca−nimia), parapatric (crecca−carolinensis), and (mostly) allopatric (carolinensis−flavirostris). Ultraconserved elements are a powerful tool for simultaneously studying systematics and population genomics in systems like this.

Genotypes of informative loci from 1000 Genomes data allude evolution and mixing of human populations

Principal Component Analysis (PCA) projects high-dimensional genotype data into a few components that discern populations. Ancestry Informative Markers (AIMs) are a small subset of SNPs capable of distinguishing populations. We integrate these two approaches by proposing an algorithm to identify necessary informative loci whose removal from the data deteriorates the PCA structure. Unlike classical AIMs, necessary informative loci densely cover the genome, hence can illuminate the evolution and mixing history of populations. We conduct a comprehensive analysis to the genotype data of the 1000 Genomes Project using necessary informative loci. Projections along the top seven principal components demarcate populations at distinct geographic levels. Millions of necessary informative loci along each PC are identified. Population identities along each PC are approximately determined by weighted sums of minor (or major) alleles over the informative loci. Variations of allele frequencies are aligned with the history and direction of population evolution. The population distribution of projections along the top three PCs is recapitulated by a simple demographic model based on several waves of founder population separation and mixing. Informative loci possess locational concentration in the genome and functional enrichment. Genes at two hot spots encompassing dense PC 7 informative loci exhibit differential expressions among European populations. The mosaic of local ancestry in the genome of a mixed descendant from multiple populations can be inferred from partial PCA projections of informative loci. Finally, informative loci derived from the 1000 Genomes data well predict the projections of an independent genotype data of South Asians. These results demonstrate the utility and relevance of informative loci to investigate human evolution.

The impact of genetic modifiers on variation in germline mutation rates within and among human populations

Mutation rates and spectra differ among human populations. Here, we examine whether this variation could be explained by evolution at mutation modifiers. To this end, we consider genetic modifier sites at which mutations, “mutator alleles”, increase genome-wide mutation rates and model their evolution under purifying selection due to the additional deleterious mutations that they cause, genetic drift, and demographic processes. We solve the model analytically for a constant population size and characterize how evolution at modifier sites impacts variation in mutation rates within and among populations. We then use simulations to study the effects of modifier sites under a plausible demographic model for Africans and Europeans. When comparing populations that evolve independently, weakly selected modifier sites (2Nes ≈ 1), which evolve slowly, contribute the most to variation in mutation rates. In contrast, when populations recently split from a common ancestral population, strongly selected modifier sites (2Nes ≫ 1), which evolve rapidly, contribute the most to variation between them. Moreover, a modest number of modifier sites (e.g., 10 per mutation type in the standard classification into 96 types) subject to moderate to strong selection (2Nes > 1) could account for the variation in mutation rates observed among human populations. If such modifier sites indeed underlie differences among populations, they should also cause variation in mutation rates within populations and their effects should be detectable in pedigree studies.

Contrasting genetic signal of recolonization after rainforest fragmentation in African trees with different dispersal abilities

Although today the forest cover is continuous in Central Africa, this may have not always been the case, as the scarce fossil record in this region suggests that arid conditions might have significantly reduced tree density during the ice ages. Our aim was to investigate whether the dry ice age periods left a genetic signature on tree species that can be used to infer the date of the past fragmentation of the rainforest. We sequenced reduced representation libraries of 182 samples representing five widespread legume trees and seven outgroups. Phylogenetic analyses identified an early divergent lineage for all species in West Africa (Upper Guinea) and two clades in Central Africa: Lower Guinea-North and Lower Guinea-South. As the structure separating the Northern and Southern clades—congruent across species—cannot be explained by geographic barriers, we tested other hypotheses with demographic model testing using δαδι. The best estimates indicate that the two clades split between the Upper Pliocene and the Pleistocene, a date compatible with forest fragmentation driven by ice age climatic oscillations. Furthermore, we found remarkably older split dates for the shade-tolerant tree species with nonassisted seed dispersal than for light-demanding species with long-distance wind-dispersed seeds. Different recolonization abilities after recurrent cycles of forest fragmentation seem to explain why species with long-distance dispersal show more recent genetic admixture between the two clades than species with limited seed dispersal. Despite their old history, our results depict the African rainforests as a dynamic biome where tree species have expanded relatively recently after the last glaciation.

SIA: Selection Inference Using the Ancestral Recombination Graph

Detecting signals of selection from genomic data is a central problem in population genetics. Coupling the rich information in the ancestral recombination graph (ARG) with a powerful and scalable deep learning framework, we developed a novel method to detect and quantify positive selection: Selection Inference using the Ancestral recombination graph (SIA). Built on a Long Short-Term Memory (LSTM) architecture, a particular type of a Recurrent Neural Network (RNN), SIA can be trained to explicitly infer a full range of selection coefficients, as well as the allele frequency trajectory and time of selection onset. We benchmarked SIA extensively on simulations under a European human demographic model, and found that it performs as well or better as some of the best available methods, including state-of-the-art machine-learning and ARG-based methods. In addition, we used SIA to estimate selection coefficients at several loci associated with human phenotypes of interest. SIA detected novel signals of selection particular to the European (CEU) population at the MC1R and ABCC11 loci. In addition, it recapitulated signals of selection at the LCT locus and several pigmentation-related genes. Finally, we reanalyzed polymorphism data of a collection of recently radiated southern capuchino seedeater taxa in the genus Sporophila to quantify the strength of selection and improved the power of our previous methods to detect partial soft sweeps. Overall, SIA uses deep learning to leverage the ARG and thereby provides new insight into how selective sweeps shape genomic diversity.