Biases in demographic modelling affect our understanding of recent divergence

Abstract Testing among competing demographic models of divergence has become an important component of evolutionary research in model and non-model organisms. However, the effect of unaccounted demographic events on model choice and parameter estimation remains largely unexplored. Using extensive simulations, we demonstrate that under realistic divergence scenarios, failure to account for population size (Ne) changes in daughter and ancestral populations leads to strong biases in divergence time estimates as well as model choice. We illustrate these issues reconstructing the recent demographic history of North Sea and Baltic Sea turbots (Schopthalmus maximus) by testing 16 Isolation with Migration (IM) and 16 Secondary Contact (SC) scenarios, modelling changes in Ne as well as the effects of linked selection and barrier loci. Failure to account for changes in Ne resulted in selecting SC models with long periods of isolation and divergence times preceding the formation of the Baltic Sea. In contrast, models accounting for Ne changes suggest recent (<6 kya) divergence with constant gene flow. We further show how interpreting genomic landscapes of differentiation can help discerning among competing models. For example, in the turbots data islands of differentiation show signatures of recent selective sweeps, rather than old divergence resisting secondary introgression. The results have broad implications for the study of population divergence by high-lighting the potential effects of unmodeleld changes in Ne on demographic inference. Tested models should aim at representing realistic divergence scenarios for the target taxa, and extreme caution should always be exercised when interpreting results of demographic modelling.

Download Full-text

Beyond parallel evolution: when several species colonize the same environmental gradient

10.1101/662569 ◽

2019 ◽

Cited By ~ 6

Author(s):

Alan Le Moan ◽

Oscar Gaggiotti ◽

Romina Henriques ◽

Paulino Martinez ◽

Dorte Bekkevold ◽

...

Keyword(s):

Baltic Sea ◽

Environmental Gradient ◽

Salinity Gradient ◽

Demographic History ◽

Parallel Evolution ◽

Secondary Contact ◽

Population Divergence ◽

The Baltic Sea ◽

Evolutionary Forces ◽

The Baltic

AbstractGenomic signatures associated with population divergence, speciation and the evolutionary mechanisms responsible for these are key research topics in evolutionary biology. Evolutionary radiations and parallel evolution have offered opportunities to study the role of the environment by providing replicates of ecologically driven speciation. Here, we apply an extension of the parallel evolution framework to study replicates of ecological speciation where multiple species went through a process of population divergence during the colonization of a common environmental gradient. We used the conditions offered by the North Sea – Baltic Sea environmental transition zone and found clear evidence of population structure linked to the Baltic Sea salinity gradient in four flatfish species. We found highly heterogeneous signatures of population divergence within and between species, and no evidence of parallel genomic architecture across species associated with the divergence. Analyses of demographic history suggest that Baltic Sea lineages are older than the age of the Baltic Sea itself. In most cases, divergence appears to involve reticulated demography through secondary contact, and our analyses revealed that genomic patterns of divergence were likely the result of a combination of effects from past isolation and subsequent adaptation to a new environment. In one case, we identified two large structural variants associated with the environmental gradient, where populations were inferred to have diverged in the presence of gene flow. Our results highlight the heterogeneous genomic effects associated with complex interplays of evolutionary forces, and stress the importance of genomic background for studies of parallel evolution.

Download Full-text

The demographic and adaptive history of the African green monkey

10.1101/098947 ◽

2017 ◽

Cited By ~ 1

Author(s):

Susanne P. Pfeifer

Keyword(s):

Genetic Diversity ◽

Demographic History ◽

Divergence Time ◽

African Green Monkey ◽

Population Variation ◽

Population Divergence ◽

Nucleotide Polymorphisms ◽

Divergence Time Estimates ◽

Green Monkey ◽

History Of

AbstractRelatively little is known about the evolutionary history of the African green monkey (genus Chlorocebus) due to the lack of sampled polymorphism data from wild populations. Yet, this characterization of genetic diversity is not only critical for a better understanding of their own history, but also for human biomedical research given that they are one of the most widely used primate models. Here, I analyze the demographic and selective history of the African green monkey, utilizing one of the most comprehensive catalogs of wild genetic diversity to date, consisting of 1,795,643 autosomal single nucleotide polymorphisms in 25 individuals, representing all five major populations: C. a. aethiops, C. a. cynosurus, C. a. pygerythrus, C. a. sabaeus, and C. a tantalus. Assuming a mutation rate of 5.9 × 10−9 per base pair per generation and a generation time of 8.5 years, divergence time estimates range from 523-621kya for the basal split of C. a. aethiops from the other four populations. Importantly, the resulting tree characterizing the relationship and split-times between these populations differs significantly from that presented in the original genome paper, owing to their neglect of within-population variation when calculating between population-divergence. In addition, I find that the demographic history of all five populations is well explained by a model of population fragmentation and isolation, rather than novel colonization events. Finally, utilizing these demographic models as a null, I investigate the selective history of the populations, identifying candidate regions potentially related to adaptation in response to pathogen exposure.

Download Full-text

Climatic Refugia and Geographical Isolation Contribute to the Speciation and Genetic Divergence in Himalayan-Hengduan Tree Peonies (Paeonia delavayi and Paeonia ludlowii)

Frontiers in Genetics ◽

10.3389/fgene.2020.595334 ◽

2021 ◽

Vol 11 ◽

Author(s):

Yu-Juan Zhao ◽

Gen-Shen Yin ◽

Yue-Zhi Pan ◽

Bo Tian ◽

Xun Gong

Keyword(s):

Genetic Variation ◽

Late Quaternary ◽

Demographic History ◽

Nuclear Gene ◽

Genetic Distances ◽

Population Divergence ◽

Widespread Species ◽

Isolation With Migration ◽

Isolation By Environment ◽

Paeonia Delavayi

Himalaya and Hengduan Mountains (HHM) is a biodiversity hotspot, and very rich in endemic species. Previous phylogeographical studies proposed different hypotheses (vicariance and climate-driven speciation) in explaining diversification and the observed pattern of extant biodiversity, but it is likely that taxa are forming in this area in species-specific ways. Here, we reexplored the phylogenetic relationship and tested the corresponding hypotheses within Paeonia subsect. Delavayanae composed of one widespread species (Paeonia delavayi) and the other geographically confined species (Paeonia ludlowii). We gathered genetic variation data at three chloroplast DNA fragments and one nuclear gene from 335 individuals of 34 populations sampled from HHM. We performed a combination of population genetic summary statistics, isolation-with-migration divergence models, isolation by environment, and demographic history analyses. We found evidence for the current taxonomic treatment that P. ludlowii and P. delavayi are two different species with significant genetic differentiation. The significant isolation by environment was revealed within all sampled populations but genetic distances only explained by geographical distances within P. delavayi populations. The results of population divergence models and demographic history analyses indicated a progenitor–derivative relationship and the Late Quaternary divergence without gene flow between them. The coalescence of all sampled cpDNA haplotypes could date to the Late Miocene, and P. delavayi populations probably underwent a severe bottleneck in population size during the last glacial period. Genetic variation in Paeonia subsect. Delavayanae is associated with geographical and environmental distances. These findings point to the importance of geological and climatic changes as causes of the speciation event and lineage diversification within Paeonia subsect. Delavayanae.

Download Full-text

Blockwise Site Frequency Spectra for Inferring Complex Population Histories and Recombination

10.1101/077958 ◽

2016 ◽

Cited By ~ 3

Author(s):

Champak R. Beeravolu ◽

Michael J. Hickerson ◽

Laurent A.F. Frantz ◽

Konrad Lohse

Keyword(s):

Demographic History ◽

Composite Likelihood ◽

Model Organisms ◽

Secondary Contact ◽

Parameter Estimates ◽

Genome Sequences ◽

Frequency Spectra ◽

Genome Wide ◽

Complex Population ◽

History Of

AbstractWe introduce ABLE (Approximate Blockwise Likelihood Estimation), a novel composite likelihood framework based on a recently introduced summary of sequence variation: the blockwise site frequency spectrum (bSFS). This simulation-based framework uses the the frequencies of bSFS configurations to jointly model demographic history and recombination and is explicitly designed to make inference using multiple whole genomes or genome-wide multi-locus data (e.g. RADSeq) catering to the needs of researchers studying model or non-model organisms respectively. The flexible nature of our method further allows for arbitrarily complex population histories using unphased and unpolarized whole genome sequences. In silico experiments demonstrate accurate parameter estimates across a range of divergence models with increasing complexity, and as a proof of principle, we infer the demographic history of the two species of orangutan from multiple genome sequences (over 160 Mbp in length) from each species. Our results indicate that the two orangutan species split approximately 650-950 thousand years ago but experienced a pulse of secondary contact much more recently, most likely during a period of low sea-level South East Asia (∼300,000 years ago). Unlike previous analyses we can reject a history of continuous gene flow and co-estimate genome-wide recombination. ABLE is available for download at https://github.com/champost/ABLE.

Download Full-text

Reconstructing the demographic history of divergence between European river and brook lampreys using approximate Bayesian computations

PeerJ ◽

10.7717/peerj.1910 ◽

2016 ◽

Vol 4 ◽

pp. e1910 ◽

Cited By ~ 17

Author(s):

Quentin Rougemont ◽

Camille Roux ◽

Samuel Neuenschwander ◽

Jerome Goudet ◽

Sophie Launey ◽

...

Keyword(s):

Gene Flow ◽

Life Histories ◽

Evolutionary Biology ◽

Demographic History ◽

Secondary Contact ◽

Isolation With Migration ◽

Genome Wide Data ◽

History Of ◽

Parameterized Model ◽

Approximate Bayesian

Inferring the history of isolation and gene flow during species divergence is a central question in evolutionary biology. The European river lamprey (Lampetra fluviatilis) and brook lamprey(L. planeri)show a low reproductive isolation but have highly distinct life histories, the former being parasitic-anadromous and the latter non-parasitic and freshwater resident. Here we used microsatellite data from six replicated population pairs to reconstruct their history of divergence using an approximate Bayesian computation framework combined with a random forest model. In most population pairs, scenarios of divergence with recent isolation were outcompeted by scenarios proposing ongoing gene flow, namely the Secondary Contact (SC) and Isolation with Migration (IM) models. The estimation of demographic parameters under the SC model indicated a time of secondary contact close to the time of speciation, explaining why SC and IM models could not be discriminated. In case of an ancient secondary contact, the historical signal of divergence is lost and neutral markers converge to the same equilibrium as under the less parameterized model allowing ongoing gene flow. Our results imply that models of secondary contacts should be systematically compared to models of divergence with gene flow; given the difficulty to discriminate among these models, we suggest that genome-wide data are needed to adequately reconstruct divergence history.

Download Full-text

Biases in demographic modelling affect our understanding of recent divergence

10.1101/2020.06.03.128298 ◽

2020 ◽

Cited By ~ 1

Author(s):

Paolo Momigliano ◽

Ann-Britt Florin ◽

Juha Merilä

Keyword(s):

Gene Flow ◽

Baltic Sea ◽

North Sea ◽

Secondary Contact ◽

Model Choice ◽

The Baltic Sea ◽

The North ◽

The North Sea ◽

Constant Gene ◽

The Baltic

Estimating patterns of gene flow during the early stages of divergence is central to understanding whether reproductive isolation arises through gradual erosion of gene flow or via successive stages of strict isolation and secondary contact. Such scenarios can be tested by comparing the joint allele frequency spectrum (jAFS) of a set of populations to jAFS simulated under scenarios of isolation with migration (IM) and secondary contact (SC). However, the potential effect of unaccounted demographic events (such as population expansions and bottlenecks) on model choice and parameter estimation remains largely unexplored. Using simulations, we demonstrate that under realistic divergence scenarios with constant gene flow, failure to account for population size (Ne) changes in daughter and ancestral populations leads to biases in divergence time estimates as well as model choice. On the other hand, when the simulations included long periods of strict isolation the correct gene flow scenario was usually retrieved. We illustrate these issues reconstructing the recent demographic history of North Sea and Baltic Sea turbots (Schopthalmus maximus) by testing 16 IM and 16 SC scenarios, modelling changes in Ne as well as the effects of linked selection and barrier loci. Failure to account for changes in Ne resulted in selecting SC models with long periods of isolation and divergence times preceding the formation of the Baltic Sea. In contrast, models accounting for Ne changes suggest that the Baltic Sea turbot population originated from a recent (<6 kya) invasion and has diverged with constant gene flow from the North Sea. We further show how interpreting genomic landscape of differentiation can help discerning among competing models. For example, turbots show no signature of increased absolute divergence (dxy) with respect to genetic diversity in the North Sea. Two islands of high differentiation show genomic signature characteristic of recent selective sweeps, rather than old divergence resisting secondary introgression. The results have broad implications for the study of recent population divergence by high-lighting the potential effects of ancestral size changes and bottlenecks followed by growth on demographic inference. In general, extreme caution should be exercised when interpreting results of demographic mode.

Download Full-text

Reconstructing the demographic history of Atlantic Salmon (Salmo salar) across its distribution range using Approximate Bayesian Computations

10.1101/142372 ◽

2017 ◽

Cited By ~ 1

Author(s):

Quentin Rougemont ◽

Louis Bernatchez

Keyword(s):

North America ◽

Atlantic Salmon ◽

Northern Hemisphere ◽

Demographic History ◽

Secondary Contact ◽

Population Divergence ◽

Isolated Populations ◽

Quaternary Period ◽

History Of ◽

Approximate Bayesian

AbstractUnderstanding the dual roles of demographic and selective processes in the buildup of population divergence is one of the most challenging tasks in evolutionary biology. In the Northern hemisphere in particular, species genetic makeup has been largely influenced by severe climatic oscillations of the Quaternary Period. Here, we investigated the demographic history of Atlantic Salmon across the entire species range using 2035 anadromous individuals from 77 sampling sites from North America and Eurasia genotyped at 4,656 SNPs. By combining results from admixture graphs, geogenetic maps and an approximate Bayesian computation framework, we validate previous hypotheses pertaining to secondary contact between European and Northern American populations, but also demonstrate that European populations from different glacial refugia have been exchanging alleles in contemporary times. We further identify the major sources of admixture from the southern range of North America to more northern populations along with a strong signal of secondary gene flow between genetic regional groups. We hypothesize that these patterns reflects the spatial redistribution of ancestral variation across the entire American range. Results also point to a role for linked selection in the form of background selection and or positive hitchhiking. Altogether, differential introgression and linked selective effects likely played an underappreciated role in shaping the genomic landscape of species in the Northern hemisphere Therefore we conclude that such heterogeneity among loci should be systematically integrated into demographic inferences of the divergence process, even between incompletely reproductively isolated populations.

Download Full-text

PipeMaster: inferring population divergence and demographic history with approximate Bayesian computation and supervised machine-learning in R

10.1101/2020.12.04.410670 ◽

2020 ◽

Author(s):

Marcelo Gehara ◽

Guilherme G. Mazzochinni ◽

Frank Burbrink

Keyword(s):

Machine Learning ◽

Approximate Bayesian Computation ◽

Demographic History ◽

Divergence Time ◽

R Package ◽

Supervised Machine Learning ◽

Population Divergence ◽

Bayesian Computation ◽

Approximate Bayesian ◽

Recent Bottleneck

AbstractUnderstanding population divergence involves testing diversification scenarios and estimating historical parameters, such as divergence time, population size and migration rate. There is, however, an immense space of possible highly parameterized scenarios that are difsficult or impossible to solve analytically. To overcome this problem researchers have used alternative simulation-based approaches, such as approximate Bayesian computation (ABC) and supervised machine learning (SML), to approximate posterior probabilities of hypotheses. In this study we demonstrate the utility of our newly developed R-package to simulate summary statistics to perform ABC and SML inferences. We compare the power of both ABC and SML methods and the influence of the number of loci in the accuracy of inferences; and we show three empirical examples: (i) the Muller’s termite frog genomic data from Southamerica; (ii) the cottonmouth and (iii) and the copperhead snakes sanger data from Northamerica. We found that SML is more efficient than ABC. It is generally more accurate and needs fewer simulations to perform an inference. We found support for a divergence model without migration, with a recent bottleneck for one of the populations of the southamerican frog. For the cottonmouth we found support for divergence with migration and recent expansion and for the copperhead we found support for a model of divergence with migration and recent bottleneck. Interestingly, by using an SML method it was possible to achieve high accuracy in model selection even when several models were compared in a single inference. We also found a higher accuracy when inferring parameters with SML.

Download Full-text

Molecular phylogeny and divergence time estimates of Penaeid Shrimp Lineages (Decapoda: Penaeidae)

Zootaxa ◽

10.11646/zootaxa.2107.1.2 ◽

2009 ◽

Vol 2107 (1) ◽

pp. 41-52 ◽

Cited By ~ 5

Author(s):

CAROLINA M VOLOCH ◽

PABLO R FREIRE ◽

CLAUDIA A M RUSSO

Keyword(s):

Fossil Record ◽

Divergence Time ◽

Penaeid Shrimp ◽

Divergence Time Estimates ◽

Time Estimates ◽

Global Clock ◽

Late Tertiary ◽

The Family ◽

Molecular Studies ◽

Triassic Period

Fossil record of penaeids indicates that the family exists since the Triassic period, but extant genera appeared only recently in Tertiary strata. Molecular based divergence time estimates on the matter of penaeid radiation were never properly addressed, due to shortcomings of the global molecular clock assumptions. Here, we studied the diversification patterns of the family, uncovering, more specifically, a correlation between fossil and extant Penaeid fauna. For this, we have used a Bayesian framework that does not assume a global clock. Our results suggest that Penaeid genera originated between 20 million years ago and 43 million years ago, much earlier than expected by previous molecular studies. Altogether, these results promptly discard late Tertiary or even Quaternary hypotheses that presumed a major glaciations influence on the diversification patterns of the family.

Download Full-text

Out of the Neotropics: Late Cretaceous colonization of Australasia by American arthropods

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2012.0675 ◽

2012 ◽

Vol 279 (1742) ◽

pp. 3501-3509 ◽

Cited By ~ 41

Author(s):

Prashant P. Sharma ◽

Gonzalo Giribet

Keyword(s):

Late Cretaceous ◽

Divergence Time ◽

Disjunct Distribution ◽

Continental Margins ◽

Divergence Time Estimates ◽

Evolutionary Origins ◽

Source Regions ◽

Time Estimates ◽

Fiji Islands ◽

The Pacific

The origins of tropical southwest Pacific diversity are traditionally attributed to southeast Asia or Australia. Oceanic and fragment islands are typically colonized by lineages from adjacent continental margins, resulting in attrition of diversity with distance from the mainland. Here, we show that an exceptional tropical family of harvestmen with a trans-Pacific disjunct distribution has its origin in the Neotropics. We found in a multi-locus phylogenetic analysis that the opilionid family Zalmoxidae, which is distributed in tropical forests on both sides of the Pacific, is a monophyletic entity with basal lineages endemic to Amazonia and Mesoamerica. Indo-Pacific Zalmoxidae constitute a nested clade, indicating a single colonization event. Lineages endemic to putative source regions, including Australia and New Guinea, constitute derived groups. Divergence time estimates and probabilistic ancestral area reconstructions support a Neotropical origin of the group, and a Late Cretaceous ( ca 82 Ma) colonization of Australasia out of the Fiji Islands and/or Borneo, which are consistent with a transoceanic dispersal event. Our results suggest that the endemic diversity within traditionally defined zoogeographic boundaries might have more complex evolutionary origins than previously envisioned.

Download Full-text