Section: Evolutionary Biology
Topic:
Evolution,
Genetics/Genomics,
Population biology
Introgression between highly divergent sea squirt genomes: an adaptive breakthrough?
Corresponding author(s): Fraïsse, Christelle (christelle.fraisse@univ-lille.fr)
10.24072/pcjournal.172 - Peer Community Journal, Volume 2 (2022), article no. e54.
Get full text PDF Peer reviewed and recommended by PCIHuman-mediated introductions are reshuffling species distribution on a global scale. Consequently, an increasing number of allopatric taxa are now brought into contact, promoting introgressive hybridization between incompletely isolated species and new adaptive gene transfer. The broadcast spawning marine species, Ciona robusta, has been recently introduced in the native range of its sister taxa, Ciona intestinalis, in the English Channel and North-East Atlantic. These sea squirts are highly divergent, yet hybridization has been reported by crossing experiments and genetic studies in the wild. Here, we examined the consequences of secondary contact between C. intestinalis and C. robusta in the English Channel. We produced genomes phased by transmission to infer the history of divergence and gene flow, and analyzed introgressed genomic tracts. Demographic inference revealed a history of secondary contact with a low overall rate of introgression. Introgressed tracts were short, segregating at low frequency, and scattered throughout the genome, suggesting traces of past contacts during the last 30 ky. However, we also uncovered a hotspot of introgression on chromosome 5, characterized by several hundred kb-long C. robusta haplotypes segregating in C. intestinalis, that introgressed during contemporary times the last 75 years. Although locally more frequent than the baseline level of introgression, C. robusta alleles are not fixed, even in the core region of the introgression hotspot. Still, linkage-disequilibrium patterns and haplotype-based tests suggest this genomic region is under recent positive selection. We further detected in the hotspot an over-representation of candidate SNPs lying on a cytochrome P450 gene with a high copy number of tandem repeats in the introgressed alleles. Cytochromes P450 are a superfamily of enzymes involved in detoxifying exogenous compounds, constituting a promising avenue for functional studies. These findings support that introgression of an adaptive allele is possible between very divergent genomes and that anthropogenic hybridization can provide the raw material for adaptation of native lineages in the Anthropocene.
Type: Research article
Fraïsse, Christelle 1, 2; Le Moan, Alan 3, 4; Roux, Camille 1; Dubois, Guillaume 3; Daguin-Thiebaut, Claire 3; Gagnaire, Pierre-Alexandre 2; Viard, Frédérique 2, 3; Bierne, Nicolas 2
@article{10_24072_pcjournal_172, author = {Fra{\"\i}sse, Christelle and Le Moan, Alan and Roux, Camille and Dubois, Guillaume and Daguin-Thiebaut, Claire and Gagnaire, Pierre-Alexandre and Viard, Fr\'ed\'erique and Bierne, Nicolas}, title = {Introgression between highly divergent sea squirt genomes: an adaptive breakthrough?}, journal = {Peer Community Journal}, eid = {e54}, publisher = {Peer Community In}, volume = {2}, year = {2022}, doi = {10.24072/pcjournal.172}, url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.172/} }
TY - JOUR AU - Fraïsse, Christelle AU - Le Moan, Alan AU - Roux, Camille AU - Dubois, Guillaume AU - Daguin-Thiebaut, Claire AU - Gagnaire, Pierre-Alexandre AU - Viard, Frédérique AU - Bierne, Nicolas TI - Introgression between highly divergent sea squirt genomes: an adaptive breakthrough? JO - Peer Community Journal PY - 2022 VL - 2 PB - Peer Community In UR - https://peercommunityjournal.org/articles/10.24072/pcjournal.172/ DO - 10.24072/pcjournal.172 ID - 10_24072_pcjournal_172 ER -
%0 Journal Article %A Fraïsse, Christelle %A Le Moan, Alan %A Roux, Camille %A Dubois, Guillaume %A Daguin-Thiebaut, Claire %A Gagnaire, Pierre-Alexandre %A Viard, Frédérique %A Bierne, Nicolas %T Introgression between highly divergent sea squirt genomes: an adaptive breakthrough? %J Peer Community Journal %D 2022 %V 2 %I Peer Community In %U https://peercommunityjournal.org/articles/10.24072/pcjournal.172/ %R 10.24072/pcjournal.172 %F 10_24072_pcjournal_172
Fraïsse, Christelle; Le Moan, Alan; Roux, Camille; Dubois, Guillaume; Daguin-Thiebaut, Claire; Gagnaire, Pierre-Alexandre; Viard, Frédérique; Bierne, Nicolas. Introgression between highly divergent sea squirt genomes: an adaptive breakthrough?. Peer Community Journal, Volume 2 (2022), article no. e54. doi : 10.24072/pcjournal.172. https://peercommunityjournal.org/articles/10.24072/pcjournal.172/
PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.evolbiol.100149
Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.
[1] Contrasting global genetic patterns in two biologically similar, widespread and invasive Ciona species (Tunicata, Ascidiacea), Scientific Reports, Volume 6 (2016) no. 1 | DOI
[2] Co-occurrence and reproductive synchrony do not ensure hybridization between an alien tunicate and its interfertile native congener, Evolutionary Ecology, Volume 30 (2016) no. 1, pp. 69-87 | DOI
[3] Distinguishing contemporary hybridization from past introgression with postgenomic ancestry-informative SNPs in strongly differentiated Ciona species, Molecular Ecology, Volume 25 (2016) no. 21, pp. 5527-5542 | DOI
[4] Do settlement dynamics influence competitive interactions between an alien tunicate and its native congener?, Ecology and Evolution, Volume 7 (2017) no. 1, pp. 200-213 | DOI
[5] Rapid and Accurate Haplotype Phasing and Missing-Data Inference for Whole-Genome Association Studies By Use of Localized Haplotype Clustering, The American Journal of Human Genetics, Volume 81 (2007) no. 5, pp. 1084-1097 | DOI
[6] Morphological evidence that the molecularly determined Ciona intestinalis type A and type B are different species: Ciona robusta and Ciona intestinalis, Journal of Zoological Systematics and Evolutionary Research, Volume 53 (2015) no. 3, pp. 186-193 | DOI
[7] Selection and hybridization shaped the rapid spread of African honey bee ancestry in the Americas, PLOS Genetics, Volume 16 (2020) no. 10 | DOI
[8] The variant call format and VCFtools, Bioinformatics, Volume 27 (2011) no. 15, pp. 2156-2158 | DOI
[9] SweepFinder2: increased sensitivity, robustness and flexibility, Bioinformatics, Volume 32 (2016) no. 12, pp. 1895-1897 | DOI
[10] The origin and remolding of genomic islands of differentiation in the European sea bass, Nature Communications, Volume 9 (2018) no. 1 | DOI
[11] Supplementary Data of "Introgression between highly divergent sea squirt genomes: an adaptive breakthrough?" [Data set], Zenodo, 2022 | DOI
[12] Supplementary Information of "Introgression between highly divergent sea squirt genomes: an adaptive breakthrough?" (Version 1) [Data set], Zenodo, 2022
[13] DILS: Demographic inferences with linked selection by using ABC, Molecular Ecology Resources, Volume 21 (2021) no. 8, pp. 2629-2644 | DOI
[14] The divergence history of European blue mussel species reconstructed from Approximate Bayesian Computation: the effects of sequencing techniques and sampling strategies, PeerJ, Volume 6 (2018) | DOI
[15] A New Method to Scan Genomes for Introgression in a Secondary Contact Model, PLOS ONE, Volume 10 (2015) no. 4 | DOI
[16] A Draft Sequence of the Neandertal Genome, Science, Volume 328 (2010) no. 5979, pp. 710-722 | DOI
[17] Anthropogenic transport of species across native ranges: unpredictable genetic and evolutionary consequences, Biology Letters, Volume 12 (2016) no. 10 | DOI
[18] Application of Phylogenetic Networks in Evolutionary Studies, Molecular Biology and Evolution, Volume 23 (2006) no. 2, pp. 254-267 | DOI
[19] Inferring the Joint Demographic History of Multiple Populations: Beyond the Diffusion Approximation, Genetics, Volume 206 (2017) no. 3, pp. 1549-1567 | DOI
[20] Chromosome–size dependent control of meiotic recombination in humans, Nature Genetics, Volume 13 (1996) no. 1, pp. 20-21 | DOI
[21] Stepwise evolution of a butterfly supergene via duplication and inversion, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 377 (2022) no. 1856 | DOI
[22] The Fate of Mutations Surfing on the Wave of a Range Expansion, Molecular Biology and Evolution, Volume 23 (2006) no. 3, pp. 482-490 | DOI
[23] Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 375 (2020) no. 1806 | DOI
[24] An introgression breakthrough left by an anthropogenic contact between two ascidians, Molecular Ecology, Volume 30 (2021) no. 24, pp. 6718-6732 | DOI
[25] Fast and accurate short read alignment with Burrows-Wheeler transform, Bioinformatics, Volume 25 (2009) no. 14, pp. 1754-1760 | DOI
[26] Genetic variation associated with increased insecticide resistance in the malaria mosquito, Anopheles coluzzii, Parasites & Vectors, Volume 11 (2018) no. 1 | DOI
[27] Coupling molecular data and experimental crosses sheds light about species delineation: a case study with the genus Ciona, Scientific Reports, Volume 8 (2018) no. 1 | DOI
[28] Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci, Molecular Biology and Evolution, Volume 32 (2015) no. 1, pp. 244-257 | DOI
[29] Interpreting the genomic landscape of introgression, Current Opinion in Genetics & Development, Volume 47 (2017), pp. 69-74 | DOI
[30] An integrative taxonomic framework for the study of the genus Ciona (Ascidiacea) and description of a new species, Ciona intermedia, Zoological Journal of the Linnean Society, Volume 19 (2020), pp. 1193-1216 | DOI
[31] Gene exchange between two divergent species of the fungal human pathogen, Coccidioides, Evolution, Volume 73 (2019) no. 1, pp. 42-58 | DOI
[32] Detecting the True Extent of Introgression during Anthropogenic Hybridization, Trends in Ecology & Evolution, Volume 34 (2019) no. 4, pp. 315-326 | DOI
[33] The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data, Genome Research, Volume 20 (2010) no. 9, pp. 1297-1303 | DOI
[34] The genomic consequences of hybridization, eLife, Volume 10 (2021) | DOI
[35] Mathematical model for studying genetic variation in terms of restriction endonucleases., Proceedings of the National Academy of Sciences, Volume 76 (1979) no. 10, pp. 5269-5273 | DOI
[36] Metazoan cytochrome P450 evolution, Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology, Volume 121 (1998) no. 1-3, pp. 15-22 | DOI
[37] Genomewide analysis of admixture and adaptation in the Africanized honeybee, Molecular Ecology, Volume 26 (2017) no. 14, pp. 3603-3617 | DOI
[38] YASS: enhancing the sensitivity of DNA similarity search, Nucleic Acids Research, Volume 33 (2005) no. Web Server | DOI
[39] Insights into invasive species from whole‐genome resequencing, Molecular Ecology, Volume 30 (2021) no. 23, pp. 6289-6308 | DOI
[40] Genealogical relationships within and among shallow-water Ciona species (Ascidiacea), Marine Biology, Volume 151 (2007) no. 5, pp. 1839-1847 | DOI
[41] Polymorphism and divergence within the ascidian genus Ciona, Molecular Phylogenetics and Evolution, Volume 56 (2010) no. 2, pp. 718-726 | DOI
[42] Introgression despite substantial divergence in a broadcast spawning marine invertebrate, Evolution, Volume 65 (2011) no. 2, pp. 429-442 | DOI
[43] PLINK: A Tool Set for Whole-Genome Association and Population-Based Linkage Analyses, The American Journal of Human Genetics, Volume 81 (2007) no. 3, pp. 559-575 | DOI
[44] The genic view of hybridization in the Anthropocene, Evolutionary Applications, Volume 14 (2021) no. 10, pp. 2342-2360 | DOI
[45] Ancient Admixture in Human History, Genetics, Volume 192 (2012) no. 3, pp. 1065-1093 | DOI
[46] Amplification of a Cytochrome P450 Gene Is Associated with Resistance to Neonicotinoid Insecticides in the Aphid Myzus persicae, PLoS Genetics, Volume 6 (2010) no. 6 | DOI
[47] Evidence for archaic adaptive introgression in humans, Nature Reviews Genetics, Volume 16 (2015) no. 6, pp. 359-371 | DOI
[48] The genomic landscape at a late stage of stickleback speciation: High genomic divergence interspersed by small localized regions of introgression, PLOS Genetics, Volume 14 (2018) no. 5 | DOI
[49] Integrative genomics viewer, Nature Biotechnology, Volume 29 (2011) no. 1, pp. 24-26 | DOI
[50] Shedding Light on the Grey Zone of Speciation along a Continuum of Genomic Divergence, PLOS Biology, Volume 14 (2016) no. 12 | DOI
[51] Crossing the Species Barrier: Genomic Hotspots of Introgression between Two Highly Divergent Ciona intestinalis Species, Molecular Biology and Evolution, Volume 30 (2013) no. 7, pp. 1574-1587 | DOI
[52] Detecting recent positive selection in the human genome from haplotype structure, Nature, Volume 419 (2002) no. 6909, pp. 832-837 | DOI
[53] Introgression of a Block of Genome Under Infinitesimal Selection, Genetics, Volume 209 (2018) no. 4, pp. 1279-1303 | DOI
[54] Adaptively introgressed Neandertal haplotype at the OAS locus functionally impacts innate immune responses in humans, Genome Biology, Volume 17 (2016) no. 1 | DOI
[55] Field identification of ‘types’ A and B of the ascidian Ciona intestinalis in a region of sympatry, Marine Biology, Volume 159 (2012) no. 7, pp. 1611-1619 | DOI
[56] A Nearly Complete Genome of Ciona intestinalis Type A (C. robusta) Reveals the Contribution of Inversion to Chromosomal Evolution in the Genus Ciona, Genome Biology and Evolution, Volume 11 (2019) no. 11, pp. 3144-3157 | DOI
[57] Copy Number Variation and Transposable Elements Feature in Recent, Ongoing Adaptation at the Cyp6g1 Locus, PLoS Genetics, Volume 6 (2010) no. 6 | DOI
[58] VolcanoFinder: Genomic scans for adaptive introgression, PLOS Genetics, Volume 16 (2020) no. 6 | DOI
[59] Evolution of strong reproductive isolation in plants: broad-scale patterns and lessons from a perennial model group, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 375 (2020) no. 1806 | DOI
[60] Global Diversity of Ascidiacea, PLoS ONE, Volume 6 (2011) no. 6 | DOI
[61] Chromosomal mapping of 170 BAC clones in the ascidian Ciona intestinalis, Genome Research, Volume 16 (2006) no. 2, pp. 297-303 | DOI
[62] Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels, Evolutionary Applications, Volume 13 (2020) no. 3, pp. 575-599 | DOI
[63] Linking climate change and biological invasions: Ocean warming facilitates nonindigenous species invasions, Proceedings of the National Academy of Sciences, Volume 99 (2002) no. 24, pp. 15497-15500 | DOI
[64] The evolution of strong reproductive isolation between sympatric intertidal snails, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 375 (2020) no. 1806 | DOI
[65] Genome Patterns of Selection and Introgression of Haplotypes in Natural Populations of the House Mouse (Mus musculus), PLoS Genetics, Volume 8 (2012) no. 8 | DOI
[66] Selscan 2.0: scanning for sweeps in unphased data, biorxiv (2021) | DOI
[67] Evolutionary relationship of DNA sequences in finite populations, Genetics, Volume 105 (1983) no. 2, pp. 437-460 | DOI
[68] Urban rendezvous along the seashore: Ports as Darwinian field labs for studying marine evolution in the Anthropocene, Evolutionary Applications, Volume 00 (2022), pp. 1-20 | DOI
[69] Ghost Lineages Highly Influence the Interpretation of Introgression Tests, Systematic Biology, Volume 71 (2022) no. 5, pp. 1147-1158 | DOI
[70] The Population Genomics of a Fast Evolver: High Levels of Diversity, Functional Constraint, and Molecular Adaptation in the Tunicate Ciona intestinalis, Genome Biology and Evolution, Volume 4 (2012) no. 8, pp. 852-861 | DOI
[71] Fine scale mapping of genomic introgressions within the Drosophila yakuba clade, PLOS Genetics, Volume 13 (2017) no. 9 | DOI
[72] Adaptive Introgression across Semipermeable Species Boundaries between Local Helicoverpa zea and Invasive Helicoverpa armigera Moths, Molecular Biology and Evolution, Volume 37 (2020) no. 9, pp. 2568-2583 | DOI
[73] From FastQ Data to High‐Confidence Variant Calls: The Genome Analysis Toolkit Best Practices Pipeline, Current Protocols in Bioinformatics, Volume 43 (2013) no. 1 | DOI
[74] Anthropogenic hybridization at sea: three evolutionary questions relevant to invasive species management, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 375 (2020) no. 1806 | DOI
[75] Transcriptomic Analyses Reveal 2 and 4 Family Members of Cytochromes P450 (CYP) Involved in LPS Inflammatory Response in Pharynx of Ciona robusta, International Journal of Molecular Sciences, Volume 22 (2021) no. 20 | DOI
[76] Estimating F-Statistics for the Analysis of Population Structure, Evolution, Volume 38 (1984) no. 6 | DOI
[77] Two duplicated P450 genes are associated with pyrethroid resistance in Anopheles funestus, a major malaria vector, Genome Research, Volume 19 (2009) no. 3, pp. 452-459 | DOI
[78] Geographic Monitoring of Insecticide Resistance Mutations in Native and Invasive Populations of the Fall Armyworm, Insects, Volume 12 (2021) no. 5 | DOI
[79] Genome-wide patterns of divergence and introgression after secondary contact between Pungitius sticklebacks, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 375 (2020) no. 1806 | DOI
[80] Ascidians as models for studying invasion success, Marine Biology, Volume 162 (2015) no. 12, pp. 2449-2470 | DOI
[81] Invasion genetics of the Ciona intestinalis species complex: from regional endemism to global homogeneity, Molecular Ecology, Volume 19 (2010) no. 21, pp. 4678-4694 | DOI
[82] Neofunctionalization of Duplicated P450 Genes Drives the Evolution of Insecticide Resistance in the Brown Planthopper, Current Biology, Volume 28 (2018) no. 2 | DOI
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