Barrier Loci and Evolution

Abstract

The evolution and maintenance of new species is a major question in evolutionary biology. During speciation, the genomes of individuals in the splitting populations do not diverge at an equal rate: some parts diverge more quickly while other parts remain more similar. The organisation of genetic diversity and differentiation in the genome is important to how speciation happens and reflective of speciation processes. Barrier loci are parts of the genome that contribute to a restriction of gene flow at that genomic region and are most diverged between young species. The size and distribution of barrier loci is influenced by evolutionary processes such as demography, selection, and gene flow, and by properties of the genome such as mutation rate, gene density, and recombination. Speciation research is in an exciting new era of identifying barrier loci and their distribution in the genome and testing what they reveal about the processes of evolution.

Key Concepts

  • As populations become more different with divergence and speciation, the rate and pattern at which genetic differences accumulate are not the same across the genome.
  • Barrier loci are those loci that resist homogenisation with the other genome when gene flow occurs between diverging species, and consequently, they are the most different parts of the genome between divergent populations.
  • Genomic divergence is affected by many properties of the genome and of the species being studied, and therefore the process of divergence and the effects on barrier loci are complex and variable.
  • Barrier loci form due to a reduction in gene flow at particular genomic regions. Therefore, they are a function of both population factors (demography, time since divergence, and strength and target of selection) and properties of the genome (recombination rate, mutation rate, gene density, and the organisation of relevant loci).
  • Barrier loci are inferred with genome‚Äźwide molecular methods and analytical tools.
  • Barrier loci give important insights into the genetic basis of species differences and the process and rates of speciation.

Keywords: speciation; genomics; population genetics; gene flow; reproductive isolation

Figure 1. The genomic landscape of barrier loci: expectations under sympatric divergence (a) vs secondary contact (b). These are only schematics. As divergence happens with high levels of gene flow (a) or with periods of isolation (b) (gene flow shown in blue arrows), speciation occurs for example from dark grey medium‐sized ancestral fish species to light grey thin‐bodied and black high‐bodied contemporary fish species. The background genome will be more divergent (higher Fst or genetic differentiation) under secondary contact and therefore make it more difficult to accurately infer functional barrier loci.
close

References

Barrett RDH and Schluter D (2008) Adaptation from standing genetic variation. Trends in Ecology & Evolution 23: 38–44.

Bernatchez L , Renaut S , Whiteley AR , et al. (2010) On the origin of species: insights from the ecological genomics of the lake whitefish. Philosophical Transactions of the Royal Society of London, Series B 365: 1783–1800.

Burri R , Nater A , Kawakami T , et al. (2015) Linked selection and recombination rate variation drive the evolution of the genomic landscape of differentiation across the speciation continuum of Ficedula flycatchers. Genome Research 25: 1656–1665.

Butlin RK (2005) Recombination and speciation. Molecular Ecology 14: 2621–2635.

Butlin RK (2010) Population genomics and speciation. Genetica 138: 409–418.

Charlesworth B (2009) Effective population size and patterns of molecular evolution and variation. Nature Reviews. Genetics 10: 195–207.

Coyne JA and Orr HA (2004) Speciation. Sunderland: Sinauer Associates, Inc.

Cruickshank TE and Hahn MW (2014) Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Molecular Ecology 23: 3133–3157.

Davey JW , Hohenlohe PA , Etter PD , et al. (2011) Genome‐wide genetic marker discovery and genotyping using next‐generation sequencing. Nature Reviews. Genetics 12: 499–510.

Elmer KR , Lehtonen TK , Kautt A , Harrod C and Meyer A (2010) Rapid sympatric ecological differentiation of crater lake cichlid fishes in historic times. BMC Biology 8: 60.

Elmer KR and Meyer A (2011) Adaptation in the age of ecological genomics: insights from parallelism and convergence. Trends in Ecology & Evolution 26: 298–306.

Elmer KR (2016) Genomic tools for new insights to variation, adaptation, and evolution in the salmonid fishes: a perspective for charr. Hydrobiologia 783: 191–208.

Felsenstein J (1981) Skepticism towards Santa Rosalia, or why are there so few kinds of animals? Evolution 35: 124–138.

Foote AD (2018) Sympatric speciation in the genomic era. Trends in Ecology & Evolution 33: 85–95.

Hermisson J and Pennings PS (2005) Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 169: 2335–2352.

Jacobs A , Hughes MR , Robinson PC , Adams CE and Elmer KR (2018) The genetic architecture underlying the evolution of a rare piscivorous life history form in brown trout after secondary contact and strong introgression. Genes 9: 280.

Jensen JD (2014) On the unfounded enthusiasm for soft selective sweeps. Nature Communications 5: 5281.

Jones FC , Grabherr MG , Chan YF , et al. (2012) The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484: 55–61.

Kautt AF , Machado‐Schiaffino G and Meyer A (2016) Multispecies outcomes of sympatric speciation after admixture with the source population in two radiations of Nicaraguan crater lake cichlids. PLoS Genetics 12: e1006157.

Kitano J , Bolnick DI , Beauchamp DA , et al. (2008) Reverse evolution of armor plates in the threespine stickleback. Current Biology 18: 769–774.

Lescak EA , Bassham SL , Catchen J , et al. (2015) Evolution of stickleback in 50 years on earthquake‐uplifted islands. Proceedings of the National Academy of Sciences of the United States of America 112: E7204–E7212.

Nichols R (2001) Gene trees and species trees are not the same. Trends in Ecology & Evolution 16: 358–364.

Nosil P , Funk DJ and Ortiz‐Barrientos D (2009) Divergent selection and heterogeneous genomic divergence. Molecular Ecology 18: 375–402.

Nosil P (2012) Ecological Speciation. Cambridge: Oxford University Press.

Paccard A , Wasserman BA , Hanson D , et al. (2018) Adaptation in temporally variable environments: stickleback armor in periodically breaching bar‐built estuaries. Journal of Evolutionary Biology 31: 735–752.

Payseur BA and Nachman MW (2002) Gene density and human nucleotide polymorphism. Molecular Biology and Evolution 19: 336–340.

Ravinet M , Faria R , Butlin RK , et al. (2017) Interpreting the genomic landscape of speciation: a road map for finding barriers to gene flow. Journal of Evolutionary Biology 30: 1450–1477.

Reid NM , Proestou DA , Clark BW , et al. (2016) The genomic landscape of rapid repeated evolutionary adaptation to toxic pollution in wild fish. Science 354: 1305–1308.

Seehausen O , Butlin RK , Keller I , et al. (2014) Genomics and the origin of species. Nature Reviews. Genetics 15: 176–192.

Sodeland M , Jorde PE , Lien S , et al. (2016) “Islands of divergence” in the Atlantic Cod genome represent polymorphic chromosomal rearrangements. Genome Biology and Evolution 8: 1012–1022.

Stapley J , Reger J , Feulner PGD , et al. (2010) Adaptation genomics: the next generation. Trends in Ecology & Evolution 25: 705–712.

Storz JF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Molecular Ecology 14: 671–688.

Turner TL , Hahn MW and Nuzhdin SV (2005) Genomic islands of speciation in Anopheles gambiae . PLoS Biology 3: 1572.

Wu CI (2001) The genic view of the process of speciation. Journal of Evolutionary Biology 14: 851–865.

Yeaman S and Whitlock MC (2011) The genetic architecture of adaptation under migration–selection balance. Evolution 65: 1897–1911.

Yeaman S (2013) Genomic rearrangements and the evolution of clusters of locally adaptive loci. Proceedings of the National Academy of Sciences of the United States of America 110: E1743–E1751.

Yeaman S , Aeschbacher S and Burger R (2016) The evolution of genomic islands by increased establishment probability of linked alleles. Molecular Ecology 25: 2542–2558.

Further Reading

Coyne JA and Orr HA (2004) Speciation. Sunderland: Sinauer Associates, Inc.

Ellegren H (2014) Genome sequencing and population genomics in non‐model organisms. Trends in Ecology & Evolution 29: 51–63.

Feder JL , Egan SP and Nosil P (2012) The genomics of speciation‐with‐gene‐flow. Trends in Genetics 28: 342–350.

Rice AM , Rudh A , Ellegren H and Qvarnström A (2011) A guide to the genomics of ecological speciation in natural animal populations. Ecology Letters 14: 9–18.

Ravinet M , Faria R , Butlin RK , et al. (2017) Interpreting the genomic landscape of speciation: a road map for finding barriers to gene flow. Journal of Evolutionary Biology 30: 1450–1477.

Seehausen O , Butlin RK , Keller I , et al. (2014) Genomics and the origin of species. Nature Reviews. Genetics 15: 176–192.

Wolf JB and Ellegren H (2017) Making sense of genomic islands of differentiation in light of speciation. Nature Reviews. Genetics 18: 87–100.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Elmer, Kathryn R(Feb 2019) Barrier Loci and Evolution. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0028138]