Genetic variation in Pan species is shaped by demographic history and underlies lineage-specific functions

AbstractChimpanzees (Pan troglodytes) and bonobos (Pan paniscus) are the closest living relatives of humans, but they show distinct behavioral and physiological differences, particularly regarding female reproduction. Despite their recent rapid decline, the demographic histories of the two species have been different during the past one to two million years, likely having an impact on their genomic diversity. Here, we analyze the inferred functional consequences of genetic variation across 69 individuals, making use of the most complete dataset of genomic variation in the Pan clade to date. We test to which extent the demographic history influences the efficacy of purifying selection in these species. We find that small historical effective population sizes (Ne) correlate not only with small genetic diversity, but also with more homozygous deleterious alleles, and an increased proportion of deleterious changes at low frequencies. Furthermore, we exploit the catalog of deleterious protein-coding changes on each lineage to investigate the putative genetic basis for phenotypic differences between chimpanzees and bonobos. We show that bonobo-specific non-synonymous changes are enriched in genes related to age at menarche in humans, suggesting that the prominent physiological differences in the female reproductive system between chimpanzees and bonobos might be explained, in part, by putatively adaptive changes on the bonobo lineage.

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Chromosome-level assembly of the Atlantic silverside genome reveals extreme levels of sequence diversity and structural genetic variation

10.1101/2020.10.27.357293 ◽

2020 ◽

Author(s):

Anna Tigano ◽

Arne Jacobs ◽

Aryn P. Wilder ◽

Ankita Nand ◽

Ye Zhan ◽

...

Keyword(s):

Genetic Variation ◽

Structural Variation ◽

Demographic History ◽

Genome Structure ◽

Genomic Variation ◽

Adaptive Divergence ◽

Effective Population ◽

Atlantic Silverside ◽

A Genome ◽

Chromosome Level

AbstractThe levels and distribution of standing genetic variation in a genome can provide a wealth of insights about the adaptive potential, demographic history, and genome structure of a population or species. As structural variants are increasingly associated with traits important for adaptation and speciation, investigating both sequence and structural variation is essential for wholly tapping this potential. Using a combination of shotgun sequencing, 10X Genomics linked reads and proximity-ligation data (Chicago and Hi-C), we produced and annotated a chromosome-level genome assembly for the Atlantic silverside (Menidia menidia) - an established ecological model for studying the phenotypic effects of natural and artificial selection - and examined patterns of genomic variation across two individuals sampled from different populations with divergent local adaptations. Levels of diversity varied substantially across each chromosome, consistently being highly elevated near the ends (presumably near telomeric regions) and dipping to near zero around putative centromeres. Overall, our estimate of the genome-wide average heterozygosity in the Atlantic silverside is the highest reported for a fish, or any vertebrate, to date (1.32-1.76% depending on inference method and sample). Furthermore, we also found extreme levels of structural variation, affecting ~23% of the total genome sequence, including multiple large inversions (> 1 Mb and up to 12.6 Mb) associated with previously identified haploblocks showing strong differentiation between locally adapted populations. These extreme levels of standing genetic variation are likely associated with large effective population sizes and may help explain the remarkable adaptive divergence among populations of the Atlantic silverside.

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The great tit HapMap project: a continental-scale analysis of genomic variation in a songbird

10.1101/561399 ◽

2019 ◽

Cited By ~ 3

Author(s):

Lewis G. Spurgin ◽

Mirte Bosse ◽

Frank Adriaensen ◽

Tamer Albayrak ◽

Christos Barboutis ◽

...

Keyword(s):

Positive Selection ◽

Recombination Rate ◽

Demographic History ◽

Great Tit ◽

Genomic Variation ◽

Genomic Diversity ◽

Hapmap Project ◽

Widespread Species ◽

Continental Scale ◽

Genome Wide

AbstractA major aim of evolutionary biology is to understand why patterns of genomic diversity vary among populations and species. Large-scale genomic studies of widespread species are useful for studying how the environment and demographic history shape patterns of genomic divergence, and with the continually decreasing cost of sequencing and genotyping, such studies are now becoming feasible. Here, we carry out one of the most geographically comprehensive surveys of genomic variation in a wild vertebrate to date; the great tit (Parus major) HapMap project. We screened ca 500,000 SNP markers across 647 individuals from 29 populations, spanning almost the entire geographic range of the European great tit subspecies. We found that genome-wide variation was consistent with a recent colonisation across Europe from a single refugium in South-East Europe, with bottlenecks and reduced genetic diversity in island populations. Differentiation across the genome was highly heterogeneous, with clear “islands of differentiation” even among populations with very low levels of genome-wide differentiation. Low local recombination rate in the genome was a strong predictor of high local genomic differentiation (FST), especially in island and peripheral mainland populations, suggesting that the interplay between genetic drift and recombination is a key driver of highly heterogeneous differentiation landscapes. We also detected genomic outlier regions that were confined to one or more peripheral great tit populations, most likely as a result of recent directional selection at the range edges of this species. Haplotype-based measures of selection were also related to recombination rate, albeit less strongly, and highlighted population-specific sweeps that likely resulted from positive selection. These regions under positive selection contained candidate genes associated with morphology, thermal adaptation and colouration, providing promising avenues for future investigation. Our study highlights how comprehensive screens of genomic variation in wild organisms can provide unique insights into evolution.

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Spatial, climate, and ploidy factors drive genomic diversity and resilience in the widespread grass Themeda triandra

10.1101/864298 ◽

2019 ◽

Author(s):

CW Ahrens ◽

EA James ◽

AD Miller ◽

NC Aitken ◽

JO Borevitz ◽

...

Keyword(s):

Genetic Variation ◽

Isolation By Distance ◽

Management Strategies ◽

Genomic Variation ◽

Genomic Diversity ◽

List Type ◽

Themeda Triandra ◽

Reduced Representation ◽

Isolation By Environment ◽

Susceptible Populations

SummaryFragmented grassland ecosystems, and the species that shape them, are under immense pressure. Restoration and management strategies should include genetic diversity and adaptive capacity to improve success but these data are generally unavailable. Therefore, we use the foundational grass, Themeda triandra, to test how spatial, environmental, and ploidy factors shape patterns of genetic variation.We used reduced-representation genome sequencing on 487 samples from 52 locations to answer fundamental questions about how the distribution of genomic diversity and ploidy polymorphism supports adaptation to harsher climates. We explicitly quantified isolation-by-distance (IBD), isolation-by-environment (IBE), and predicted population genomic vulnerability in 2070.We found that a majority (54%) of the genomic variation could be attributed to IBD, while 22% of the genomic variation could be explained by four climate variables showing IBE. Results indicate that heterogeneous patterns of vulnerability across populations are due to genetic variation, multiple climate factors, and ploidy polymorphism, which lessened genomic vulnerability in the most susceptible populations.These results indicate that restoration and management of T. triandra should incorporate knowledge of genomic diversity and ploidy polymorphisms to increase the likelihood of population persistence and restoration success in areas that will become hotter and more arid.

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Adaptive Radiation Genomics of Two Ecologically Divergent Hawai‘ian Honeycreepers: The ‘akiapōlā‘au and the Hawai‘i ‘amakihi

Journal of Heredity ◽

10.1093/jhered/esz057 ◽

2019 ◽

Cited By ~ 1

Author(s):

Michael G Campana ◽

André Corvelo ◽

Jennifer Shelton ◽

Taylor E Callicrate ◽

Karen L Bunting ◽

...

Keyword(s):

Adaptive Radiation ◽

De Novo ◽

Demographic History ◽

Genomic Islands ◽

Genomic Diversity ◽

Morphology Evolution ◽

Effective Population ◽

Island Endemic ◽

Wide Range ◽

Bill Morphology

Abstract The Hawai‘ian honeycreepers (drepanids) are a classic example of adaptive radiation: they adapted to a variety of novel dietary niches, evolving a wide range of bill morphologies. Here we investigated genomic diversity, demographic history, and genes involved in bill morphology phenotypes in 2 honeycreepers: the ‘akiapōlā‘au (Hemignathus wilsoni) and the Hawai‘i ‘amakihi (Chlorodrepanis virens). The ‘akiapōlā‘au is an endangered island endemic, filling the “woodpecker” niche by using a unique bill morphology, while the Hawai‘i ‘amakihi is a dietary generalist common on the islands of Hawai‘i and Maui. We de novo sequenced the ‘akiapōlā‘au genome and compared it to the previously sequenced ‘amakihi genome. The ‘akiapōlā‘au is far less heterozygous and has a smaller effective population size than the ‘amakihi, which matches expectations due to its smaller census population and restricted ecological niche. Our investigation revealed genomic islands of divergence, which may be involved in the honeycreeper radiation. Within these islands of divergence, we identified candidate genes (including DLK1, FOXB1, KIF6, MAML3, PHF20, RBP1, and TIMM17A) that may play a role in honeycreeper adaptations. The gene DLK1, previously shown to influence Darwin’s finch bill size, may be related to honeycreeper bill morphology evolution, while the functions of the other candidates remain unknown.

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Ocean-wide genomic variation in Gray's beaked whales, Mesoplodon grayi

Royal Society Open Science ◽

10.1098/rsos.201788 ◽

2021 ◽

Vol 8 (3) ◽

Author(s):

M. V. Westbury ◽

K. F. Thompson ◽

M. Louis ◽

A. A. Cabrera ◽

M. Skovrind ◽

...

Keyword(s):

Population Structure ◽

Demographic History ◽

South Australia ◽

Population Connectivity ◽

Genomic Variation ◽

Suitable Habitat ◽

Effective Population ◽

Beaked Whales ◽

Marine Megafauna ◽

Demographic Patterns

The deep oceans of the Southern Hemisphere are home to several elusive and poorly studied marine megafauna. In the absence of robust observational data for these species, genetic data can aid inferences on population connectivity, demography and ecology. A previous investigation of genetic diversity and population structure in Gray's beaked whale ( Mesoplodon grayi ) from Western Australia and New Zealand found high levels of mtDNA diversity, no geographic structure and stable demographic history. To further investigate phylogeographic and demographic patterns across their range, we generated complete mitochondrial and partial nuclear genomes of 16 of the individuals previously analysed and included additional samples from South Africa ( n = 2) and South Australia ( n = 4), greatly expanding the spatial range of genomic data for the species. Gray's beaked whales are highly elusive and rarely observed, and our data represents a unique and geographically broad dataset. We find relatively high levels of diversity in the mitochondrial genome, despite an absence of population structure at the mitochondrial and nuclear level. Demographic analyses suggest these whales existed at stable levels over at least the past 1.1 million years, with an approximately twofold increase in female effective population size approximately 250 thousand years ago, coinciding with a period of increased Southern Ocean productivity, sea surface temperature and a potential expansion of suitable habitat. Our results suggest that Gray's beaked whales are likely to be resilient to near-future ecosystem changes, facilitating their conservation. Our study demonstrates the utility of low-effort shotgun sequencing in providing ecological information on highly elusive species.

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Genomic stability through time despite decades of exploitation in cod on both sides of the Atlantic

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2025453118 ◽

2021 ◽

Vol 118 (15) ◽

pp. e2025453118

Author(s):

Malin L. Pinsky ◽

Anne Maria Eikeset ◽

Cecilia Helmerson ◽

Ian R. Bradbury ◽

Paul Bentzen ◽

...

Keyword(s):

Atlantic Cod ◽

Sequence Data ◽

Genomic Variation ◽

Whole Genome Sequence ◽

Phenotypic Change ◽

Rapid Decline ◽

Effective Population ◽

Genomic Change ◽

Early 21St Century ◽

Intensive Exploitation

The mode and extent of rapid evolution and genomic change in response to human harvesting are key conservation issues. Although experiments and models have shown a high potential for both genetic and phenotypic change in response to fishing, empirical examples of genetic responses in wild populations are rare. Here, we compare whole-genome sequence data of Atlantic cod (Gadus morhua) that were collected before (early 20th century) and after (early 21st century) periods of intensive exploitation and rapid decline in the age of maturation from two geographically distinct populations in Newfoundland, Canada, and the northeast Arctic, Norway. Our temporal, genome-wide analyses of 346,290 loci show no substantial loss of genetic diversity and high effective population sizes. Moreover, we do not find distinct signals of strong selective sweeps anywhere in the genome, although we cannot rule out the possibility of highly polygenic evolution. Our observations suggest that phenotypic change in these populations is not constrained by irreversible loss of genomic variation and thus imply that former traits could be reestablished with demographic recovery.

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Fine-scale population structure and demographic history of British Pakistanis

Nature Communications ◽

10.1038/s41467-021-27394-2 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Elena Arciero ◽

Sufyan A. Dogra ◽

Daniel S. Malawsky ◽

Massimo Mezzavilla ◽

Theofanis Tsismentzoglou ◽

...

Keyword(s):

Population Structure ◽

Disease Risk ◽

Demographic History ◽

Population History ◽

Genomic Diversity ◽

Fine Scale ◽

Effective Population ◽

Scale Population ◽

The Impact ◽

British Pakistanis

AbstractPrevious genetic and public health research in the Pakistani population has focused on the role of consanguinity in increasing recessive disease risk, but little is known about its recent population history or the effects of endogamy. Here, we investigate fine-scale population structure, history and consanguinity patterns using genotype chip data from 2,200 British Pakistanis. We reveal strong recent population structure driven by the biraderi social stratification system. We find that all subgroups have had low recent effective population sizes (Ne), with some showing a decrease 15‒20 generations ago that has resulted in extensive identity-by-descent sharing and homozygosity, increasing the risk of recessive disorders. Our results from two orthogonal methods (one using machine learning and the other coalescent-based) suggest that the detailed reporting of parental relatedness for mothers in the cohort under-represents the true levels of consanguinity. These results demonstrate the impact of cultural practices on population structure and genomic diversity in Pakistanis, and have important implications for medical genetic studies.

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Genetic Diversity and Identification of Homozygosity-Rich Genomic Regions in Seven Italian Heritage Turkey (Meleagris gallopavo) Breeds

Genes ◽

10.3390/genes12091342 ◽

2021 ◽

Vol 12 (9) ◽

pp. 1342

Author(s):

Francesca Bernini ◽

Alessandro Bagnato ◽

Stefano Paolo Marelli ◽

Luisa Zaniboni ◽

Silvia Cerolini ◽

...

Keyword(s):

Genetic Variation ◽

Target Selection ◽

Meleagris Gallopavo ◽

Principal Component ◽

Genomic Diversity ◽

Effective Population ◽

A Genome ◽

Founder Populations ◽

Genomic Regions

Italian autochthonous turkey breeds are an important reservoir of genetic biodiversity that should be maintained with an in vivo approach. The aim of this study, part of the TuBAvI national project on biodiversity, was to use run of homozygosity (ROH), together with others statistical approaches (e.g., Wright’s F-statistics, principal component analysis, ADMIXTURE analysis), to investigate the genomic diversity in several heritage turkey breeds. We performed a genome-wide characterization of ROH-rich regions in seven autochthonous turkey breeds, i.e., Brianzolo (Brzl), Bronzato Comune Italiano (BrCI), Bronzato dei Colli Euganei (CoEu), Parma e Piacenza (PrPc), Nero d’Italia (NeIt), Ermellinato di Rovigo (ErRo) and Romagnolo (Roma). ROHs were detected based on a 650K SNP genotyping. ROH_islands were identified as homozygous ROH regions shared by at least 75% of birds (within breed). Annotation of genes was performed with DAVID. The admixture analyses revealed that six breeds are unique populations while the Roma breed consists in an admixture of founder populations. Effective population size estimated on genomic data shows a numeric contraction. ROH_islands harbour genes that may be interesting for target selection in commercial populations also. Among them the PTGS2 and PLA2G4A genes on chr10 were related to reproduction efficiency. This is the first study mapping genetic variation in autochthonous turkey populations. Breeds were genetically different among them, with the Roma breed proving to be a mixture of the other breeds. The ROH_islands identified harboured genes peculiar to the selection that occurred in heritage breeds. Finally, this study releases previously undisclosed information on existing genetic variation in the turkey species.

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Impact of past climate warming on genomic diversity and demographic history of collared lemmings across the Eurasian Arctic

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1913596117 ◽

2020 ◽

Vol 117 (6) ◽

pp. 3026-3033 ◽

Cited By ~ 4

Author(s):

Vadim B. Fedorov ◽

Emiliano Trucchi ◽

Anna V. Goropashnaya ◽

Eric Waltari ◽

Susan Erin Whidden ◽

...

Keyword(s):

Climate Warming ◽

Demographic History ◽

Genomic Diversity ◽

Northern Eurasia ◽

Last Interglacial ◽

Effective Population ◽

The West ◽

Past Climate ◽

History Of ◽

Late Pleistocene To Holocene

The Arctic climate was warmer than today at the last interglacial and the Holocene thermal optimum. To reveal the impact of past climate-warming events on the demographic history of an Arctic specialist, we examined both mitochondrial and nuclear genomic variation in the collared lemming (Dicrostonyx torquatus, Pallas), a keystone species in tundra communities, across its entire distribution in northern Eurasia. The ancestral phylogenetic position of the West Beringian group and divergence time estimates support the hypothesis of continental range contraction to a single refugial area located in West Beringia during high-magnitude warming of the last interglacial, followed by westward recolonization of northern Eurasia in the last glacial period. The West Beringian group harbors the highest mitogenome diversity and its inferred demography indicates a constantly large effective population size over the Late Pleistocene to Holocene. This suggests that northward forest expansion during recent warming of the Holocene thermal optimum did not affect the gene pool of the collared lemming in West Beringia but reduced genomic diversity and effective population size in all other regions of the Eurasian Arctic. Demographic inference from genomic diversity was corroborated by species distribution modeling showing reduction in species distribution during past climate warming. These conclusions are supported by recent paleoecological evidence suggesting smaller temperature increases and moderate northward forest advances in the extreme northeast of Eurasia during the Late Pleistocene-to-Holocene warming events. This study emphasizes the importance of West Beringia as a potential refugium for cold-adapted Arctic species under ongoing climate warming.

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Fine-scale population structure and demographic history of British Pakistanis

10.1101/2020.09.02.279190 ◽

2020 ◽

Author(s):

Elena Arciero ◽

Sufyan A. Dogra ◽

Massimo Mezzavilla ◽

Theofanis Tsismentzoglou ◽

Qin Qin Huang ◽

...

Keyword(s):

Population Structure ◽

Disease Risk ◽

Demographic History ◽

Population History ◽

Genomic Diversity ◽

Fine Scale ◽

Effective Population ◽

Scale Population ◽

The Impact ◽

British Pakistanis

AbstractPrevious genetic and public health research in the Pakistani population has focused on the role of consanguinity in increasing recessive disease risk, but little is known about its recent population history or the effects of endogamy. Here, we investigate fine-scale population structure, history and consanguinity patterns using genetic and questionnaire data from >4,000 British Pakistani individuals, mostly with roots in Azad Kashmir and Punjab. We reveal strong recent population structure driven by the biraderi social stratification system. We find that all subgroups have had low effective population sizes (Ne) over the last 50 generations, with some showing a decrease in Ne 15-20 generations ago that has resulted in extensive identity-by-descent sharing and increased homozygosity. Using new theory, we show that the footprint of regions of homozygosity in the two largest subgroups is about twice that expected naively based on the self-reported consanguinity rates and the inferred historical Ne trajectory. These results demonstrate the impact of the cultural practices of endogamy and consanguinity on population structure and genomic diversity in British Pakistanis, and have important implications for medical genetic studies.

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