BMC Evolutionary Biology | |
Speciation in Western Scrub-Jays, Haldane’s rule, and genetic clines in secondary contact | |
John E McCormack5  T Caleb Warr1  Brant C Faircloth4  A Townsend Peterson2  Carla Cicero3  James M Maley5  Fiona C Gowen5  | |
[1] Museum of Natural Science, Louisiana State University, Baton Rouge, LA, USA;Biodiversity Institute, University of Kansas, Lawrence, KS, USA;Museum of Vertebrate Zoology, University of California, Berkeley, CA, USA;Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA, USA;Moore Laboratory of Zoology, Occidental College, Los Angeles, CA, USA | |
关键词: Phylogeography; Postzygotic reproductive isolation; Gene flow; Speciation; Birds; | |
Others : 855228 DOI : 10.1186/1471-2148-14-135 |
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received in 2014-03-11, accepted in 2014-06-04, 发布年份 2014 |
【 摘 要 】
Background
Haldane’s Rule, the tendency for the heterogametic sex to show reduced fertility in hybrid crosses, can obscure the signal of gene flow in mtDNA between species where females are heterogametic. Therefore, it is important when studying speciation and species limits in female-heterogametic species like birds to assess the signature of gene flow in the nuclear genome as well. We studied introgression of microsatellites and mtDNA across a secondary contact zone between coastal and interior lineages of Western Scrub-Jays (Aphelocoma californica) to test for a signature of Haldane’s Rule: a narrower cline of introgression in mtDNA compared to nuclear markers.
Results
Our initial phylogeographic analysis revealed that there is only one major area of contact between coastal and interior lineages and identified five genetic clusters with strong spatial structuring: Pacific Slope, Interior US, Edwards Plateau (Texas), Northern Mexico, and Southern Mexico. Consistent with predictions from Haldane’s Rule, mtDNA showed a narrower cline than nuclear markers across a transect through the hybrid zone. This result is not being driven by female-biased dispersal because neutral diffusion analysis, which included estimates of sex-specific dispersal rates, also showed less diffusion of mtDNA. Lineage-specific plumage traits were associated with nuclear genetic profiles for individuals in the hybrid zone, indicating that these differences are under genetic control.
Conclusions
This study adds to a growing list of studies that support predictions of Haldane’s Rule using cline analysis of multiple loci of differing inheritance modes, although alternate hypotheses like selection on different mtDNA types cannot be ruled out. That Haldane’s Rule appears to be operating in this system suggests a measure of reproductive isolation between the Pacific Slope and interior lineages. Based on a variety of evidence from the phenotype, ecology, and genetics, we recommend elevating three lineages to species level: A. californica (Pacific Slope); A. woodhouseii (Interior US plus Edwards Plateau plus Northern Mexico); A. sumichrasti (Southern Mexico). The distinctive Edwards Plateau population in Texas, which was monophyletic in mtDNA except for one individual, should be studied in greater detail given habitat threat.
【 授权许可】
2014 Gowen et al.; licensee BioMed Central Ltd.
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【 图 表 】
Fig. 4.
【 参考文献 】
- [1]Edwards SV: Is a new and general theory of molecular systematics emerging? Evolution 2009, 63:1-19.
- [2]Maddison WP: Gene trees in species trees. Syst Biol 1997, 46:523-536.
- [3]Wu C-I: The genic view of the process of speciation. J Evol Biol 2001, 14:851-865.
- [4]Zink RM, Barrowclough GF: Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 2008, 17:2107-2121.
- [5]Ballard JWO, Whitlock MC: The incomplete natural history of mitochondria. Mol Ecol 2004, 13:729-744.
- [6]Haldane JBS: Sex ratio and unisexual sterility in hybrid animals. J Genet 1922, 12:101-109.
- [7]Schilthuizen M, Giesbers M, Beukeboom L: Haldane’s rule in the 21st century. Heredity 2011, 107:95-102.
- [8]Wu C-I, Johnson NA, Palopoli MF: Haldane’s rule and its legacy: why are there so many sterile males? Trends Ecol Evol 1996, 11:281-284.
- [9]Orr HA: Haldane’s rule. Annu Rev Ecol Syst 1997, 28:195-218.
- [10]Turelli M, Orr HA: The dominance theory of Haldane’s rule. Genetics 1995, 140:389-402.
- [11]Carling MD, Brumfield RT: Haldane’s rule in an avian system: using cline theory and divergence population genetics to test for differential introgression of mitochondrial, autosomal, and sex-linked loci across the Passerina bunting hybrid zone. Evolution 2008, 62:2600-2615.
- [12]Naisbit RE, Jiggins CD, Linares M, Salazar C, Mallet J: Hybrid sterility, Haldane’s rule and speciation in Heliconius cydno and H melpomene. Genetics 2002, 161:1517-1526.
- [13]Tegelström H, Gelter HP: Haldane’s rule and sex biased gene flow between two hybridizing flycatcher species (Ficedula albicollis and F. hypoleuca, Aves: Muscicapidae). Evolution 1990, 44:2012-2021.
- [14]Irwin DE, Brelsford A, Toews DPL, MacDonald C, Phinney M: Extensive hybridization in a contact zone between MacGillivray’s warblers Oporornis tolmiei and mourning warblers O. philadelphia detected using molecular and morphological analyses. J Avian Biol 2009, 40:539-552.
- [15]Carling MD, Lovette IJ, Brumfield RT: Historical divergence and gene flow: coalescent analyses of mitochondrial, autosomal and sex-linked loci in Passerina buntings. Evolution 2010, 64:1762-1772.
- [16]Kingston SE, Jernigan RW, Fagan WF, Braun D, Braun MJ: Genomic variation in cline shape across a hybrid zone. Ecol Evol 2012, 2:2737-2748.
- [17]Sætre GP, Borge T, Lindell J, Moum T, Primmer CR, Sheldon BC, Haavie J, Johnsen A, Ellegren H: Speciation, introgressive hybridization and nonlinear rate of molecular evolution in flycatchers. Mol Ecol 2001, 10:737-749.
- [18]Sætre G-P, Borge T, Lindroos K, Haavie J, Sheldon BC, Primmer C, Syvänen A-C: Sex chromosome evolution and speciation in Ficedula flycatchers. Proc R Soc Lond Ser B Biol Sci 2003, 270:53-59.
- [19]Mayr E: Systematics and the Origin of Species: From the Viewpoint of a Zoologist. Cambridge, Massachusetts: Harvard University Press; 1942.
- [20]Sangster G: The application of species criteria in avian taxonomy and its implications for the debate over species concepts. Biol Rev 2014, 89:199-214.
- [21]Toews DPL, Brelsford A: The biogeography of mitochondrial and nuclear discordance in animals. Mol Ecol 2012, 21:3907-3930.
- [22]Rheindt FE, Edwards SV: Genetic introgression: an integral but neglected component of speciation in birds. Auk 2011, 128:620-632.
- [23]Delaney KS, Zafar S, Wayne RK: Genetic divergence and differentiation within the Western Scrub-Jay (Aphelocoma californica). Auk 2008, 125:839-849.
- [24]McCormack JE, Heled J, Delaney KS, Peterson AT, Knowles LL: Calibrating divergence times on species trees versus gene trees: implications for speciation history of Aphelocoma jays. Evolution 2011, 65:184-202.
- [25]Pitelka FA: Speciation and Ecologic Distribution in American Jays of the Genus Aphelocoma. Berkeley and Los Angeles, California: University of California Press; 1951.
- [26]Peterson AT: Phylogeny and rates of molecular evolution in the Aphelocoma jays (Corvidae). Auk 1992, 109:133-147.
- [27]Bardwell E, Benkman CW, Gould WR: Adaptive geographic variation in Western Scrub-Jays. Ecology 2001, 82:2617-2627.
- [28]Peterson AT: Adaptive geographical variation in bill shape of scrub jays (Aphelocoma coerulescens). Am Nat 1993, 142:508-527.
- [29]Chesser RT, Banks RC, Barker FK, Cicero C, Dunn JL, Kratter AW, Lovette IJ, Rasmussen PC, Remsen JV Jr, Rising JD: Fifty-first supplement to the American Ornithologists’ Union check-list of North American birds. Auk 2010, 127:726-744.
- [30]Gowen F, Maley J, Cicero C, Peterson A, Faircloth B, Warr T, McCormack J: Data from: Speciation in Western Scrub-Jays, Haldane’s rule, and genetic clines in secondary contact. Dryad Digital Repository 2014. http://dx.doi.org/10.5061/dryad.57f48 webcite
- [31]Curry RL, Peterson AT, Langen TA: Western Scrub-Jay (Aphelocoma californica). The Birds of North America. Edited by Poole A. Ithaca, NY: Cornell Lab of Ornithology;
- [32]Yuri T, Jernigan RW, Brumfield RT, Bhagabati NK, Braun MJ: The effect of marker choice on estimated levels of introgression across an avian (Pipridae: Manacus) hybrid zone. Mol Ecol 2009, 18:4888-4903.
- [33]Sætre G-P, Saether SA: Ecology and genetics of speciation in Ficedula flycatchers. Mol Ecol 2010, 19:1091-1106.
- [34]Spellman GM, Riddle B, Klicka J: Phylogeography of the Mountain Chickadee (Poecile gambeli): diversification, introgression, and expansion in response to Quaternary climate change. Mol Ecol 2007, 16:1055-1068.
- [35]Cicero C: Sibling species of titmice in the Parus inornatus complex (Aves: Paridae). Univ Calif Press Publ Zoology 1996., 128
- [36]Zellmer AJ, Knowles LL: Disentangling the effects of historic vs. contemporary landscape structure on population genetic divergence. Mol Ecol 2009, 18:3593-3602.
- [37]Klicka J, Spellman GM, Winker K, Chua V, Smith BT: A phylogeographic and population genetic analysis of a widespread, sedentary North American bird: the Hairy Woodpecker (Picoides villosus). Auk 2011, 128:346-362.
- [38]Spellman GM, Klicka J: Phylogeography of the White-breasted Nuthatch (Sitta carolinensis): diversification in North American pine and oak woodlands. Mol Ecol 2007, 16:1729-1740.
- [39]Betancourt JL, Van Devender TR, Martin PPS: Packrat Middens: The Last 40,000 Years of Biotic Change. Tucson, Arizona: University of Arizona Press; 1990.
- [40]Lucas LK, Gompert Z, Ott JR, Nice CC: Geographic and genetic isolation in spring-associated Eurycea salamanders endemic to the Edwards Plateau region of Texas. Conserv Genet 2009, 10:1309-1319.
- [41]Bowles DE, Arsuffi TL: Karst aquatic ecosystems of the Edwards Plateau region of central Texas, USA: a consideration of their importance, threats to their existence, and efforts for their conservation. Aquat Conserv Mar Freshwat Ecosyst 1993, 3:317-329.
- [42]McCormack JE, Smith TB: Niche expansion leads to small-scale adaptive divergence along an elevation gradient in a medium-sized passerine bird. Proc R Soc B 2008, 275:2155-2164.
- [43]Peterson AT: New distributional information on the Aphelocoma jays. Bull Br Ornithol Club 1991, 111:28-33.
- [44]Miller AH: The avifauna of the Sierra del Carmen of Coahuila, Mexico. Condor 1955, 57:154-178.
- [45]Peterson AT, Martinez-Meyer E, Gonzalez-Salazar C: Reconstructing the Pleistocene geography of the Aphelocoma jays (Corvidae). Divers Distrib 2004, 10:237-246.
- [46]Navarro-Sigüenza AG, Peterson AT: An alternative species taxonomy of the birds of Mexico. Biota Neotrop 2004, 4:1-32.
- [47]Burt DB, Peterson AT: Biology of cooperative-breeding Scrub Jays (Aphelocoma coerulescens) of Oaxaca, Mexico. Auk 1993, 110:207-214.
- [48]Stenzler LM, Fitzpatrick JW: Isolation of microsatellite loci in the Florida scrub-jay Aphelocoma coerulescens. Mol Ecol Notes 2002, 2:547-550.
- [49]McCormack JE, Peterson AT, Bonaccorso E, Smith TB: Speciation in the highlands of Mexico: genetic and phenotypic divergence in the Mexican jay (Aphelocoma ultramarina). Mol Ecol 2008, 17:2505-2521.
- [50]van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P: Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 2004, 4:535-538.
- [51]Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics 2000, 155:945-959.
- [52]Evanno G, Regnaut S, Goudet J: Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 2005, 14:2611-2620.
- [53]Waples RS, Gaggiotti O: Invited review: what is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 2006, 15:1419-1439.
- [54]Brown DM, Brenneman RA, Koepfli K-P, Pollinger JP, Milá B, Georgiadis NJ, Louis EE, Grether GF, Jacobs DK, Wayne RK: Extensive population genetic structure in the giraffe. BMC Biol 2007, 5:57. BioMed Central Full Text
- [55]Peterson AT: Evolutionary Relationships of the Aphelocoma Jays. University of Chicago, Committee on Evolutionary Biology; 1990.
- [56]Johnson NK: Patterns of avian geography and speciation in the Intermountain Region. Great Basin Nat Mem 1978, 2:137-159.
- [57]Drummond AJ, Suchard MA, Xie D, Rambaut A: Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 2012, 29:1969-1973.
- [58]Nylander J: MrModeltest v2. Evolutionary Biology Centre, Uppsala University, Program distributed by the author. 2004.
- [59]Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S: Geneious v5. 4. 2010. Available from http://www.geneious.com/ webcite
- [60]Derryberry EP, Derryberry GE, Maley JM, Brumfield RT: HZAR: hybrid zone analysis using an R software package. Mol Ecol Resour 2014, 14:652-66361.
- [61]Szymura JM, Barton NH: Genetic analysis of a hybrid zone between the fire-bellied toads, Bombina bombina and B. variegate, near Cracow in southern Poland. Evolution 1986, 40:1141-1159.
- [62]Szymura JM, Barton NH: The genetic structure of the hybrid zone between the fire-bellied toads Bombina bombina and B. variegata: comparisons between transects and between loci. Evolution 1991, 45:237-261.
- [63]Barton NH, Gale KS: Genetic Analysis of Hybrid Zones. In Hybrid Zones and the Evolutionary Process. Edited by Harrison RG. New York, NY: Oxford University Press; 1993.