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Review

Progress on animal speciation studies

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  • 1. State Key Laboratory for Conservation and Utilization of Bio-Resource in Yunnan, School of Life Sciences of Yunnan University, Kunming 650500, China
    2. Southwest United Graduate School, Kunming 650092, China

Received date: 2024-07-11

  Revised date: 2024-08-17

  Online published: 2024-09-19

Supported by

National Natural Science Foundation of China(31925006);Yunnan Provincial Science and Technology Project at Southwest United Graduate School(202302A0370005);Xingdian Talent Fund Project of Yunnan Province(202305AB350001)

Abstract

Speciation research represents our thinking and exploration about how new species are generated and maintained, and it is one of the most important parts of evolutionary biology. Revealing new species formation modes, processes of reproductive isolation establishment and their intrinsic genetic mechanisms, are not only important issues and primary tasks in the field of speciation, but also the key clues for our understandings about the species diversity in nature. Here, by focusing on animal groups, we first introduced different definitions of species concept, and then summarized present research progress and important breakthroughs made in the speciation modes and molecular mechanism of reproductive isolation. We also pointed out some limitations in current studies. Finally, we discuss the potential opportunities and new breakthroughs that can be made in the future studies of animal speciation.

Cite this article

Hong Wu, Yuxing Zhang, Li Yu . Progress on animal speciation studies[J]. Hereditas(Beijing), 2025 , 47(1) : 58 -70 . DOI: 10.16288/j.yczz.24-206

References

[1] Mishler BD, Brandon RN. Individuality, pluralism, and the phylogenetic species concept. Biol Philos, 1987, 2(4): 397-414.
[2] Mayden RL. On biological species, species concepts and individuation in the natural world. Fish Fish, 2002, 3(3): 171-196.
[3] Hong DY. Biodiversity pursuits need a scientific and operative species concept. Biodiversity Sci, 2016, 24(9): 979-999.
  洪德元. 生物多样性事业需要科学、可操作的物种概念. 生物多样性, 2016, 24(9): 979-999.
[4] Mayr E. Systematics and the Origin of Species from the Viewpoint of a Zoologist. New York: Columbia University Press, 1942.
[5] Paterson HEH, McEvey SF. Evolution and the Recognition Concept of Species:Collected Writings. Baltimore: Johns Hopkins University Press, 1993.
[6] Wu CI. The genic view of the process of speciation. J Evol Biol, 2001, 14(6): 851-865.
[7] Baker RJ, Bradley RD. Speciation in mammals and the genetic species concept. J Mammal, 2006, 87(4): 643-662.
[8] Van Valen L. Ecological species, multispecies, and oaks. Taxon, 1976, 25(2-3): 233-239.
[9] Simpson GG. Criteria for genera, species, and subspecies in zoology and paleozoology. Ann N Y Acad Sci, 1943, 44(2): 145-178.
[10] Simpson GG. Principles of Animal Taxonomy. New York: Columbia University Press, 1961.
[11] Wu CI, Ting CT. Genes and speciation. Nat Rev Genet, 2004, 5(2): 114-122.
[12] Liu JQ. “The integrative species concept” and “species on the speciation way”. Biodiversity Sci, 2016, 24(9): 1004-1008.
  刘建全. “整合物种概念”和“分化路上的物种”. 生物多样性, 2016, 24(9): 1004-1008.
[13] Mayr E. Animal Species and Evolution. Cambridge: Harvard University Press, 1963.
[14] Butlin RK, Galindo J, Grahame JW. Sympatric, parapatric or allopatric: the most important way to classify speciation? Philos Trans R Soc Lond B Biol Sci, 2008, 363(1506): 2997-3007.
[15] Mallet J, Meyer A, Nosil P, Feder JL. Space, sympatry and speciation. J Evol Biol, 2009, 22(11): 2332-2341.
[16] Elmer KR, Meyer A. Sympatric speciation without borders? Mol Ecol, 2010, 19(10): 1991-1993.
[17] Malay MCMD, Paulay G. Peripatric speciation drives diversification and distributional pattern of reef hermit crabs (Decapoda: Diogenidae: Calcinus). Evolution, 2010, 64(3): 634-662.
[18] Castellanos-Morales G, Gámez N, Castillo-Gámez RA, Eguiarte LE. Peripatric speciation of an endemic species driven by Pleistocene climate change: the case of the Mexican prairie dog (Cynomys mexicanus). Mol Phylogenet Evol, 2016, 94(Pt A):171-181.
[19] Gavrilets S, Li H, Vose MD. Patterns of parapatric speciation. Evolution, 2000, 54(4): 1126-1134.
[20] Bolnick DI, Fitzpatrick BM. Sympatric speciation: models and empirical evidence. Annu Rev Ecol Evol Syst, 2007, 38: 459-487.
[21] Runemark A, Vallejo-Marin M, Meier JI. Eukaryote hybrid genomes. PLoS Genet, 2019, 15(11): e1008404.
[22] Mallet J. Hybrid speciation. Nature, 2007, 446(7133): 279-283.
[23] Seehausen O. Hybridization and adaptive radiation. Trends Ecol Evol, 2004, 19(4): 198-207.
[24] Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N, Boughman J, Brelsford A, Buerkle CA, Buggs R, Butlin RK, Dieckmann U, Eroukhmanoff F, Grill A, Cahan SH, Hermansen JS, Hewitt G, Hudson AG, Jiggins C, Jones J, Keller B, Marczewski T, Mallet J, Martinez- Rodriguez P, M?st M, Mullen S, Nichols R, Nolte AW, Parisod C, Pfennig K, Rice AM, Ritchie MG, Seifert B, Smadja CM, Stelkens R, Szymura JM, V?in?l? R, Wolf JBW, Zinner D. Hybridization and speciation. J Evol Biol, 2013, 26(2): 229-246.
[25] Taylor SA, Larson EL. Insights from genomes into the evolutionary importance and prevalence of hybridization in nature. Nat Ecol Evol, 2019, 3(2): 170-177.
[26] Moran BM, Payne C, Langdon Q, Powell DL, Brandvain Y, Schumer M. The genomic consequences of hybridization. eLife, 2021, 10: e69016.
[27] Grant PR, Grant BR. Hybridization increases population variation during adaptive radiation. Proc Natl Acad Sci USA, 2019, 116(46): 23216-23224.
[28] Rieseberg LH, Carney SE. Plant hybridization. New Phytol, 1998, 140(4): 599-624.
[29] Mallet J. Hybridization as an invasion of the genome. Trends Ecol Evol, 2005, 20(5): 229-237.
[30] Marques DA, Meier JI, Seehausen O. A combinatorial view on speciation and adaptive radiation. Trends Ecol Evol, 2019, 34(6): 531-544.
[31] Pe?alba JV, Runemark A, Meier JI, Singh P, Wogan GOU, Sánchez-Guillén R, Mallet J, Rometsch SJ, Menon M, Seehausen O, Kulmuni J, Pereira RJ. The role of hybridization in species formation and persistence. Cold Spring Harb Perspect Biol, 2024, a041445.
[32] Schumer M, Rosenthal GG, Andolfatto P. How common is homoploid hybrid speciation? Evolution, 2014, 68(6): 1553-1560.
[33] Schumer M, Rosenthal GG, Andolfatto P. What do we mean when we talk about hybrid speciation? Heredity (Edinb), 2018, 120(4): 379-382.
[34] Presgraves DC. The molecular evolutionary basis of species formation. Nat Rev Genet, 2010, 11(3): 175-180.
[35] Mack KL, Nachman MW. Gene regulation and speciation. Trends Genet, 2017, 33(1): 68-80.
[36] Hermansen JS, Haas F, Trier CN, Bailey RI, Nederbragt AJ, Marzal A, S?tre GP. Hybrid speciation through sorting of parental incompatibilities in Italian sparrows. Mol Ecol, 2014, 23(23): 5831-5842.
[37] Schumer M, Cui RF, Rosenthal GG, Andolfatto P. Reproductive isolation of hybrid populations driven by genetic incompatibilities. PLoS Genet, 2015, 11(3): e1005041.
[38] Nice CC, Gompert Z, Fordyce JA, Forister ML, Lucas LK, Buerkle CA. Hybrid speciation and independent evolution in lineages of alpine butterflies. Evolution, 2013, 67(4): 1055-1068.
[39] Gompert Z, Fordyce JA, Forister ML, Shapiro AM, Nice CC. Homoploid hybrid speciation in an extreme habitat. Science, 2006, 314(5807): 1923-1925.
[40] Meier JI, Marques DA, Mwaiko S, Wagner CE, Excoffier L, Seehausen O. Ancient hybridization fuels rapid cichlid fish adaptive radiations. Nat Commun, 2017, 8: 14363.
[41] Elgvin TO, Trier CN, T?rresen OK, Hagen IJ, Lien S, Nederbragt AJ, Ravinet M, Jensen H, S?tre GP. The genomic mosaicism of hybrid speciation. Sci Adv, 2017, 3(6): e1602996.
[42] Runemark A, Trier CN, Eroukhmanoff F, Hermansen JS, Matschiner M, Ravinet M, Elgvin TO, S?tre GP. Variation and constraints in hybrid genome formation. Nat Ecol Evol, 2018, 2(3): 549-556.
[43] Jiggins CD, Salazar C, Linares M, Mavarez J. Review. Hybrid trait speciation and heliconius butterflies. Philos Trans R Soc Lond B Biol Sci, 2008, 363(1506): 3047-3054.
[44] Salazar C, Baxter SW, Pardo-Diaz C, Wu G, Surridge A, Linares M, Bermingham E, Jiggins CD. Genetic evidence for hybrid trait speciation in heliconius butterflies. PLoS Genet, 2010, 6(4): e1000930.
[45] Barrerá-Guzman AO, Aleixo A, Shawkey MD, Weir JT. Hybrid speciation leads to novel male secondary sexual ornamentation of an Amazonian bird. Proc Natl Acad Sci USA, 2018, 115(2): E218-E225.
[46] Lamichhaney S, Han F, Webster MT, Andersson L, Grant BR, Grant PR. Rapid hybrid speciation in Darwin's finches. Science, 2018, 359(6372): 224-228.
[47] Mavárez J, Salazar CA, Bermingham E, Salcedo C, Jiggins CD, Linares M. Speciation by hybridization in heliconius butterflies. Nature, 2006, 441(7095): 868-871.
[48] Meyer A, Salzburger W, Schartl M. Hybrid origin of a swordtail species (Teleostei: Xiphophorus clemenciae) driven by sexual selection. Mol Ecol, 2006, 15(3): 721-730.
[49] Wu H, Wang ZF, Zhang YX, Frantz L, Roos C, Irwin DM, Zhang CL, Liu XF, Wu DD, Huang S, Gu TT, Liu JQ, Yu L. Hybrid origin of a primate, the gray snub-nosed monkey. Science, 2023, 380(6648): eabl4997.
[50] Zhang BL, Chen W, Wang ZF, Pang W, Luo MT, Wang S, Shao Y, He WQ, Deng Y, Zhou L, Chen JW, Yang MM, Wu YJ, Wang L, Fernández-Bellon H, Molloy S, Meunier H, Wanert F, Kuderna L, Marques-Bonet T, Roos C, Qi XG, Li M, Liu ZJ, Schierup MH, Cooper DN, Liu JQ, Zheng YT, Zhang GJ, Wu DD. Comparative genomics reveals the hybrid origin of a macaque group. Sci Adv, 2023, 9(22): eadd3580.
[51] Zou TT, Kuang WM, Yin TT, Frantz L, Zhang C, Liu JQ, Wu H, Yu L. Uncovering the enigmatic evolution of bears in greater depth: the hybrid origin of the Asiatic black bear. Proc Natl Acad Sci USA, 2022, 119(31): e2120307119.
[52] Lopes F, Oliveira LR, Beux Y, Kessler A, Cárdenas- Alayza S, Majluf P, Páez-Rosas D, Chaves J, Crespo E, Brownell RL, Baylis AMM, Sepúlveda M, Franco-Trecu V, Loch C, Robertson BC, Peart CR, Wolf JBW, Bonatto SL. Genomic evidence for homoploid hybrid speciation in a marine mammal apex predator. Sci Adv, 2023, 9(18): eadf6601.
[53] Wang ZF, Kang MH, Li JL, Zhang ZY, Wang YF, Chen CL, Yang YZ, Liu JQ. Genomic evidence for homoploid hybrid speciation between ancestors of two different genera. Nat Commun, 2022, 13(1): 1987.
[54] Song C, Liu SJ, Xiao J, He WG, Zhou Y, Qin QB, Zhang C, Liu Y. Polyploid organisms. Sci China Life Sci, 2012, 55(4): 301-311.
[55] Comeault AA, Matute DR. Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation. Proc Natl Acad Sci USA, 2018, 115(39): 9761-9766.
[56] Dalbosco Dell'Aglio D, Rivas-Sánchez DF, Wright DS, Merrill RM, Montgomery SH. The sensory ecology of speciation. Cold Spring Harb Perspect Biol, 2024, 16(1): a041428.
[57] Marie Curie SPECIATION Network, Butlin R, Debelle A, Kerth C, Snook RR, Beukeboom LW, Castillo Cajas RF, Diao WW, Maan ME, Paolucci S, Weissing FJ, van de Zande L, Hoikkala A, Geuverink E, Jennings J, Kankare M, Knott KE, Tyukmaeva VI, Zoumadakis C, Ritchie MG, Barker D, Immonen E, Kirkpatrick M, Noor M, Macias Garcia C, Schmitt T, Schilthuizen M. What do we need to know about speciation? Trends Ecol Evol, 2012, 27(1): 27-39.
[58] Wiens JJ. What is speciation and how should we study it? Am Nat, 2004, 163(6): 914-923.
[59] Tomaiuolo M, Hansen TF, Levitan DR. A theoretical investigation of sympatric evolution of temporal reproductive isolation as illustrated by marine broadcast spawners. Evolution, 2007, 61(11): 2584-2595.
[60] Jezkova T, Wiens JJ. Testing the role of climate in speciation: new methods and applications to squamate reptiles (lizards and snakes). Mol Ecol, 2018, 27(12): 2754-2769.
[61] Nanda P, Singh BN. Behavioural reproductive isolation and speciation in Drosophila. J Biosci, 2012, 37(2): 359-374.
[62] Kamimura Y, Mitsumoto H. Lock-and-key structural isolation between sibling Drosophila species. Entomol Sci, 2012, 15(2): 197-201.
[63] Ludlow AM, Magurran AE. Gametic isolation in guppies (Poecilia reticulata). Proc Biol Sci, 2006, 273(1600): 2477-2482.
[64] Rosser N, Queste LM, Cama B, Edelman NB, Mann F, Mori Pezo R, Morris J, Segami C, Velado P, Schulz S, Mallet JLB, Dasmahapatra KK. Geographic contrasts between pre- and postzygotic barriers are consistent with reinforcement in Heliconius butterflies. Evolution, 2019, 73(9): 1821-1838.
[65] Rometsch SJ, Torres-Dowdall J, Meyer A. Evolutionary dynamics of pre- and postzygotic reproductive isolation in cichlid fishes. Philos Trans R Soc Lond B Biol Sci, 2020, 375(1806): 20190535.
[66] Coyne JA, Orr HA. Speciation. Sunderland, MA: Sinauer Associates Inc, 2004.
[67] Powell DL, Payne C, Banerjee SM, Keegan M, Bashkirova E, Cui R, Andolfatto P, Rosenthal GG, Schumer M. The genetic architecture of variation in the sexually selected sword ornament and its evolution in hybrid populations. Curr Biol, 2021, 31(5): 923-935.e11.
[68] Moran BM, Payne CY, Powell DL, Iverson ENK, Donny AE, Banerjee SM, Langdon QK, Gunn TR, Rodriguez- Soto RA, Madero A, Baczenas JJ, Kleczko KM, Liu F, Matney R, Singhal K, Leib RD, Hernandez-Perez O, Corbett-Detig R, Frydman J, Gifford C, Schartl M, Havird JC, Schumer M. A lethal mitonuclear incompatibility in complex I of natural hybrids. Nature, 2024, 626(7997): 119-127.
[69] Bateson B. William Bateson, Naturalist:Heredity and Variation in Modern Lights. Cambridge: Cambridge University Press, 2009, 215-232.
[70] Dobzhansky T. Genetics and the Origin of Species. New York: Columbia University Press, 1937.
[71] Maheshwari S, Barbash DA. The genetics of hybrid incompatibilities. Annu Rev Genet, 2011, 45: 331-355.
[72] Tang SW, Presgraves DC. Evolution of the Drosophila nuclear pore complex results in multiple hybrid incompatibilities. Science, 2009, 323(5915): 779-782.
[73] Presgraves DC, Balagopalan L, Abmayr SM, Orr HA. Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature, 2003, 423(6941): 715-719.
[74] Barbash DA, Siino DF, Tarone AM, Roote J. A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proc Natl Acad Sci USA, 2003, 100(9): 5302-5307.
[75] Brideau NJ, Flores HA, Wang J, Maheshwari S, Wang X, Barbash DA. Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science, 2006, 314(5803): 1292-1295.
[76] Masly JP, Jones CD, Noor MAF, Locke J, Orr HA. Gene transposition as a cause of hybrid sterility in Drosophila. Science, 2006, 313(5792): 1448-1450.
[77] Cooper JC, Lukacs A, Reich S, Schauer T, Imhof A, Phadnis N. Altered localization of hybrid incompatibility proteins in Drosophila. Mol Biol Evol, 2019, 36(8): 1783-1792.
[78] Sawamura K, Yamamoto MT, Watanabe TK. Hybrid lethal systems in the Drosophila melanogaster species complex. II. The zygotic hybrid rescue (Zhr) gene of D. melanogaster. Genetics, 1993, 133(2): 307-313.
[79] Cattani MV, Presgraves DC. Incompatibility between X chromosome factor and pericentric heterochromatic region causes lethality in hybrids between Drosophila melanogaster and its sibling species. Genetics, 2012, 191(2): 549-559.
[80] Ting CT, Tsaur SC, Wu ML, Wu CI. A rapidly evolving homeobox at the site of a hybrid sterility gene. Science, 1998, 282(5393): 1501-1504.
[81] Liénard MA, Araripe LO, Hartl DL. Neighboring genes for DNA-binding proteins rescue male sterility in Drosophila hybrids. Proc Natl Acad Sci USA, 2016, 113(29): E4200-E4207.
[82] Phadnis N. Genetic architecture of male sterility and segregation distortion in Drosophila pseudoobscura Bogota-USA hybrids. Genetics, 2011, 189(3): 1001-1009.
[83] Powell DL, García-Olazábal M, Keegan M, Reilly P, Du K, Díaz-Loyo AP, Banerjee S, Blakkan D, Reich D, Andolfatto P, Rosenthal GG, Schartl M, Schumer M. Natural hybridization reveals incompatible alleles that cause melanoma in swordtail fish. Science, 2020, 368(6492): 731-736.
[84] Mihola O, Trachtulec Z, Vlcek C, Schimenti JC, Forejt J. A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science, 2009, 323(5912): 373-375.
[85] Forejt J, Jansa P, Parvanov E. Hybrid sterility genes in mice (Mus musculus): a peculiar case of PRDM9 incompatibility. Trends Genet, 2021, 37(12): 1095-1108.
[86] Mukaj A, Piálek J, Fotopulosova V, Morgan AP, Odenthal-Hesse L, Parvanov ED, Forejt J. Prdm9 intersubspecific interactions in hybrid male sterility of house mouse. Mol Biol Evol, 2020, 37(12): 3423-3438.
[87] Johannesson K. Parallel speciation: a key to sympatric divergence. Trends Ecol Evol, 2001, 16(3): 148-153.
[88] Wang ZF, Jiang YZ, Yang XY, Bi H, Li JL, Mao XX, Ma YZ, Ru DF, Zhang C, Hao GQ, Wang J, Abbott RJ, Liu JQ. Molecular signatures of parallel adaptive divergence causing reproductive isolation and speciation across two genera. Innovation (Camb), 2022, 3(3): 100247.
[89] Butlin RK. Recombination and speciation. Mol Ecol, 2005, 14(9): 2621-2635.
[90] Bastide H, López-Villavicencio M, Ogereau D, Lledo J, Dutrillaux AM, Debat V, Llaurens V. Genome assembly of 3 Amazonian morpho butterfly species reveals Z-chromosome rearrangements between closely related species living in sympatry. Gigascience, 2022, 12: giad033.
[91] De vos JM, Augustijnen H, B?tscher L, Lucek K. Speciation through chromosomal fusion and fission in Lepidoptera. Philos Trans R Soc Lond B Biol Sci, 2020, 375(1806): 20190539.
[92] Lafon-Placette C, K?hler C. Epigenetic mechanisms of postzygotic reproductive isolation in plants. Curr Opin Plant Biol, 2015, 23: 39-44.
[93] Michalak P. Epigenetic, transposon and small RNA determinants of hybrid dysfunctions. Heredity (Edinb), 2009, 102(1): 45-50.
[94] Berbel-Filho WM, Pacheco G, Lira MG, de Leaniz CG, Lima SMQ, Rodríguez-López CM, Zhou J, Consuegra S. Additive and non-additive epigenetic signatures of natural hybridization between fish species with different mating systems. Epigenetics, 2022, 17(13): 2356-2365.
[95] Vernaz G, Hudson AG, Santos ME, Fischer B, Carruthers M, Shechonge AH, Gabagambi NP, Tyers AM, Ngatunga BP, Malinsky M, Durbin R, Turner GF, Genner MJ, Miska EA. Epigenetic divergence during early stages of speciation in an African crater lake cichlid fish. Nat Ecol Evol, 2022, 6(12): 1940-1951.
[96] Long Q, Yan K, Wang CD, Wen YL, Qi FR, Wang H, Shi P, Liu XG, Chan WY, Lu XM, Zhao H. Modification of maternally defined H3K4me3 regulates the inviability of interspecific Xenopus hybrids. Sci Adv, 2023, 9(14): eadd8343.
[97] Niayale R, Cui Y, Adzitey F. Male hybrid sterility in the cattle-yak and other bovines: a review. Biol Reprod, 2021, 104(3): 495-507.
[98] Abzhanov A, Protas M, Grant BR, Grant PR, Tabin CJ. Bmp4 and morphological variation of beaks in Darwin's finches. Science, 2004, 305(5689): 1462-1465.
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