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Allotetraploids in Patagonia with Affinities to Western North American Diploids: Did Dispersal or Genome Doubling Occur First?

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Abstract

Amphitropical disjunct distributions between western North America and western South America have intrigued botanists for over a century. Here, specific examples of migration and speciation are investigated using herbaceous species from the phlox family (Polemoniaceae) as a model for considering the timing of dispersal relative to speciation. Comparative DNA sequencing reveals that, in Collomia and Navarretia, the South American species are allopolyploids, suggesting either two dispersals prior to the allopolyploidization event for each species with subsequent extirpation of the diploid progenitors from South America, or allopolyploid formation prior to dispersal with extirpation of these polyploids from North America. Divergence time estimates support a Pliestocene dispersal hypothesis and sequence data indicate that, at least in Collomia, hybridization of the diploid progenitors occurred in South America.

Resumen

Las distribuciones anfitropicales disyuntas entre el oeste de América del Norte y el oeste de América del Sur han intrigado a los botánicos durante más de un siglo. Aquí se investigan ejemplos específicos de migración y especiación usando especies de la familia del Flox (Polemoniaceae) como un modelo para considerar el efecto del orden temporal entre dispersión y especiación. La comparación de sequencias de ADN revela que las especies sudamericanas de Navarretia y Collomia son alopoliploides y sugiere para cada una de ellas, o bien dos eventos de dispersión anteriores a la formación del alopoliploide, seguido por la desaparición de los progenitores diploides en América del Sur, o bien la formación del alopoliploide antes de la dispersión, y la extinción de los progenitores diploides en América del Norte. La estimación de los tiempos de divergencia apoya la hipótesis de una dispersión durante el Pleistoceno, y los datos de las secuencias de ADN indican que, al menos en el caso de Collomia, la hibridación de los progenitores diploides ocurrió en América del Sur.

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Acknowledgements

This research was supported by the U.S. National Science Foundation (Grants DEB-0344837, DBI-0520978, and OISE 0530267). The authors thank M. Belgrano for help with field work and specimen information from S. America, and J. M. Porter for discussions about South American Polemonioideae.

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Authors and Affiliations

  1. Department of Biology and S.L. Welsh Herbarium, Brigham Young University, Provo, UT, 84602, USA

    Leigh A. Johnson, Lauren M. Chan & Lisa D. Glazier

  2. Department of Biology, Duke University, Box 90338, Durham, NC, 27708, USA

    Lauren M. Chan

  3. Instituto de Botánica Darwinion, Casilla de Correo 22, B1642HYD San Isidro, Buenos Aires, Argentina

    Rául Pozner

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  1. Leigh A. Johnson
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Corresponding author

Correspondence to Leigh A. Johnson.

Appendix I

Appendix I

GenBank accession numbers and voucher information. Acronyms following species names correspond to those used in Figs. 2 through 5. For Collomia, genbank numbers are given in the following order: trnk, matK, trnL, trnS, psbM, ITS, PI, g3pdh. For Navarretia, the same order was followed except for g3pdh, which was not included in this study. Semicolons are used to separate genes and commas are used to separate homeologs within genes for the polyploid species. All vouchers are housed at BRY unless indicated by an alternative herbarium within brackets.

Collomia biflora (Ruiz & Pav.) Brand—ARG1 = Sersic s.n. (DQ196463; DQ196886; DQ196955; DQ196934; HQ117098; DQ196896; HQ116874, HQ116875; HQ117235, HQ117236). ARG2 = [BAA 25056] (HQ911803; HQ911925; HQ911968; HQ911789; HQ911892; HQ911836; ---, ---; HQ911783, HQ911784). ARG3 = Belgrano et al. 462 (HQ911804; HQ911926; HQ911969; HQ911790; HQ911893; HQ911837; ---, ---; ---, ---). ARG4 = Belgrano et al. 519 (HQ911806; HQ911928; HQ911971; HQ911792; HQ911895; HQ911838; ---, ---; ---, ---). ARG5 = Belgrano et al. 532 (HQ911805; HQ911927; HQ911970; HQ911791; HQ911894; HQ911839; HQ911962, HQ911963; ---,---). CHL = Thibauat et al. 156 (HQ116975; HQ116935; HQ117058; HQ117020; HQ117099; HQ116834; HQ116876, HQ116877; HQ117237, HQ117238). Collomia grandiflora Douglas ex Lindl.—AZ = Christy 449 [RSA] (HQ911808; HQ911930; HQ911973; HQ911794; HQ911897; HQ911841; ---; ---). B-ARG = Belgrano 550 (HQ911811; HQ911933; HQ911976; HQ911797; HQ911900; HQ911844; HQ911965; HQ911785). CA = Johnson 94-038 (HQ116983; HQ116942; HQ117065; HQ117027; HQ117107; HQ116840; HQ116886; HQ117247). ID = Johnson & Johnson 95-034 (HQ911809; HQ911931; HQ911974; HQ911795; HQ911898; HQ911842; HQ911966; HQ911786). OR = Johnson 93-086 (DQ196461; DQ196884; DQ196953; DQ196932; HQ117106; DQ196906; HQ116885; HQ117246). NV-1 = Johnson 04-151 (DQ196462; DQ196885; DQ196954; DQ196932; HQ117109; DQ196907; HQ116887; HQ117248). NV-2 = Howell s.n. (HQ911807; HQ911929; HQ911972; HQ911793; HQ911896; HQ911840; HQ911967; HQ911787). UT = Johnson & Matheson 03-073 (HQ911810; HQ911932; HQ911975; HQ911796; HQ911899; HQ911843; HQ911964; HQ911788). Collomia linearis Nutt.—CO-1 = Johnson 99-010 (HQ116990; HQ116947; HQ117071; HQ117032; HQ117116; HQ116845; HQ116897; HQ117258). CO-2 = Atwood & Higgins 5752 (HQ911812; HQ911934; HQ911977; HQ911798; HQ911901; HQ911845; ---; ---). ID-1 = Johnson 92-045 [WS] (HQ116988; L34188; AF208170; EU628236; EU628359; AF208200; HQ116894; HQ117255). ID-2 = Johnson 04-168 (DQ196451; DQ196874; DQ196943; DQ196922; HQ117114; DQ196895; HQ116895; HQ117256). NE = Stephens & Brooks 24521 [KANU] (HQ911814; HQ911936; HQ911979; HQ911800; ---; HQ911847; ---; ---). NV = Johnson & Johnson 04-104 (DQ196449; DQ196872; DQ196941; DQ196920; HQ117113; DQ196893; HQ116893; HQ117254). OR = Johnson 97-134 (HQ911813; HQ911935; HQ911978; HQ911799; HQ911902; HQ911846; ---; ---). UT = Thorne et al. 4171 (DQ196450; DQ196873; DQ196942; DQ196921; HQ117115; DQ196894; HQ116896; HQ117257). Collomia macrocalyx Leiberg ex Brand.—OR-1 = Johnson & Johnson 05-071 (HQ116991; HQ116948; HQ117072; HQ117033; HQ117117; HQ116846; HQ116898; HQ117259). OR-2 = Johnson & Johnson 05-079 (HQ116992; HQ116949; HQ117073; HQ117034; HQ117118; HQ116847; HQ116899; HQ117260). Collomia renacta Joyal—NV = Johnson & Johnson 04-107 (DQ196455; DQ196878; DQ196947; DQ196926; HQ117119; DQ196900; HQ116900; HQ117261). OR = Johnson & Johnson 05-103 (HQ116993; HQ116950; HQ117074; HQ117035; HQ117120; HQ116848; HQ116901; HQ117262). Collomia tenella A. Gray—NV = Johnson 06-120 (HQ116998; HQ116954; HQ117078; HQ117039; HQ117126; HQ116852; HQ116908; HQ117269). UT = Johnson 01-025 (DQ196457; DQ196880; DQ196949; DQ196928; HQ117124; DQ196902; HQ116906; HQ117267). Collomia tinctoria Kellogg—ID = Porter 13769 (DQ196445; DQ196868; DQ196937; DQ196916; HQ117130; DQ196889; HQ116912; HQ117273). OR = Johnson 95-048 (HQ117000; HQ116956; HQ117080; HQ117041; HQ117128; HQ116854; HQ116910; HQ117271). Collomia tracyi H. Mason—CA-1 = Johnson 94-075 (DQ196447; DQ196870; DQ196939; DQ196918; HQ117131; DQ196891; HQ116913; HQ117274). CA-2 = Johnson 94-078 (HQ117001; HQ116957; HQ117081; HQ911802; HQ117132; HQ116855; HQ116914; HQ117275). Collomia wilkenii L.A. Johnson & R.L. Johnson—NV1 = Johnson & Johnson 04-105 (DQ196452; DQ196875; DQ196944; DQ196923; HQ117133; DQ196908, DQ196909; HQ116915, HQ116916; HQ117276, HQ117277). NV2 = Johnson & Zhang 05-166 (HQ117002; HQ116958; HQ117082; HQ117043; HQ117134; HQ116856, HQ116857; HQ116917, HQ116918; HQ117278, HQ117279).

Navarretia fossalis Moran—CA = Spencer 4416-21 [RSA] (HQ911911; HQ912008; HQ911878; HQ911987; HQ911822; HQ911855; HQ911937). Navarretia intertexta (Benth.) Hook.—CA-1 = Johnson 93-088 (HQ911918; HQ912015; HQ911885; HQ911994; HQ911829; HQ911864; HQ911939). CA-2 = Johnson 04-038 (HQ911919; HQ912016; HQ911886; HQ911995; HQ911830; HQ911865; HQ911938). Navarretia involucrata Ruiz & Pav.—ARG-1 = Belgrano et al. 470 (HQ911907; EU628547; EU628507; EU628244; EU628367; EU628293; HQ911940, HQ911944). ARG-2 = Belgrano et al. 499 (HQ911908; HQ912005; HQ911875; HQ911984; HQ911819; HQ911852; HQ911941, HQ911943). ARG-3 = Belgrano et al. 551 (HQ911909; HQ912006; HQ911876; HQ911985; HQ911820; HQ911853; HQ911942, HQ911945). Navarretia leucocephala Benth. ssp. bakeri (H. Mason) A.G. Day—CA = Gowen 697(HQ911924; HQ912021; HQ911891; HQ912000; HQ911835; HQ911870; ---, ---). Navarretia leucocephala Benth ssp. leucocephala—CA = Johnson 04-118 (HQ911921; HQ912018; HQ911888; HQ911997; HQ911832; HQ911867; ---, ---). Navarretia leucocephala Benth. ssp. minima (Nutt.) A.G. Day—OR = Johnson 05-198 (HQ911922; HQ912019; HQ911889; HQ911998; HQ911833; HQ911868; HQ911946, HQ911947). Navarretia leucocephela ssp. pauciflora (H. Mason) A.G. Day—CA = Johnson 04-036 (HQ911923; HQ912020; HQ911890; HQ911999; HQ911834; HQ911869; HQ911960, HQ911961). Navarretia myersii P.S. Allen & A.G. Day ssp. myersii—CA = Popp s.n. [DAV] (HQ911920; HQ912017; HQ911887; HQ911996; HQ911831; HQ911866; ---, ---). Navarretia propinqua Suksd.—NV = Howell s.n. (HQ911917; HQ912014; HQ911884; HQ911993; HQ911828; HQ911862, HQ911863; HQ911948, HQ911949). UT = Johnson 04-163(HQ911916; HQ912013; HQ911883; HQ911992; HQ911827; HQ911860, HQ911861; HQ911950, HQ911951). Navarretia prostrata (A. Gray) Greene—CA = Wilken s.n. (HQ117012; HQ116967; HQ117091; HQ117052; HQ117143; HQ116866; HQ116928). Navarretia saximontana S.C. Spencer—UT = Johnson 07-036 (HQ911912; HQ912009; HQ911879; HQ911988; HQ911823; HQ911856; HQ911952, HQ911953). Navarretia sp. nov. 1—CA = Johnson et al. 09-021 (HQ911914; HQ912011; HQ911881; HQ911990; HQ911825; HQ911858; HQ911954). Navarretia sp. nov. 2—CA = Johnson et al. 09-032 (HQ911915; HQ912012; HQ911882; HQ911991; HQ911826; HQ911859; HQ911955). Navarretia sp. nov. 3—UT = Johnson & Johnson 05-197 (HQ911913; HQ912010; HQ911880; HQ911989; HQ911824; HQ911857; HQ911956). Navarretia subuligera Greene—CA-1 = Johnson & Zhang 04-135 (HQ117016; HQ116970; HQ117094; HQ117055; HQ117146; HQ116869; HQ116932). CA-2 = Johnson & Gowen 09-052 (HQ911906; HQ912004; HQ911874; HQ911983; HQ911818; HQ911851; ---). CA-3 = Spencer 568-82 [RSA] (HQ911905; HQ912003; HQ911873; HQ911982; HQ911817; HQ911850; ---). Navarretia tagetina Greene—CA-1 = Johnson 04-024 (HQ911903; HQ912001; HQ911871; HQ911980; HQ911815; HQ911848; HQ911957). CA-2 = Johnson 04-046 (HQ117017; HQ116971; HQ117095; HQ117056; HQ117147; HQ116870; HQ116933). CA-3 = Johnson & Zhang 05-164 (HQ911904; HQ912002; HQ911872; HQ911981; HQ911816; HQ911849; ---). Navarretia willamettensis S.C. Spencer—OR = Johnson & Halse 05-208 (HQ911910; HQ912007; HQ911877; HQ911986; HQ911821; HQ911854; HQ911958, HQ911959).

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Johnson, L.A., Chan, L.M., Pozner, R. et al. Allotetraploids in Patagonia with Affinities to Western North American Diploids: Did Dispersal or Genome Doubling Occur First?. Bot. Rev. 78, 288–306 (2012). https://doi.org/10.1007/s12229-012-9101-8

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