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Cryptic Host-Specific Diversity Among Western Hemisphere Broomrapes (Orobanche S.L., Orobanchaceae)

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Cryptic Host-Specific Diversity Among Western Hemisphere Broomrapes (Orobanche S.L., Orobanchaceae) Annals of Botany Page 1 of 11 doi:10.1093/aob/mcw158, available online at www.aob.oxfordjournals.org Cryptic host-specific diversity among western hemisphere broomrapes (Orobanche s.l., Orobanchaceae) Adam C. Schneider1,2,*, Alison E. L. Colwell2, Gerald M. Schneeweiss3 and Bruce G. Baldwin1,2 1Department of Integrative Biology, 1005 Valley Life Sciences Building, University of California, Berkeley, CA 94720, USA, 2Jepson Herbarium, 1001 Valley Life Sciences Building, University of California, Berkeley, CA 94720, USA and 3Department of Botany and Biodiversity Research, University of Vienna, 1030 Vienna, Austria *For correspondence. E-mail [email protected] Downloaded from Received: 30 April 2016 Returned for revision: 6 June 2016 Accepted: 24 June 2016 Background and Aims The broomrapes, Orobanche sensu lato (Orobanchaceae), are common root parasites found across Eurasia, Africa and the Americas. All species native to the western hemisphere, recognized as Orobanche sections Gymnocaulis and Nothaphyllon, form a clade that has a centre of diversity in western North America, but also includes four disjunct species in central and southern South America. The wide ecological distri- http://aob.oxfordjournals.org/ bution coupled with moderate taxonomic diversity make this clade a valuable model system for studying the role, if any, of host-switching in driving the diversification of plant parasites. Methods Two spacer regions of ribosomal nuclear DNA (ITS þ ETS), three plastid regions and one low-copy nuclear gene were sampled from 163 exemplars of Orobanche from across the native geographic range in order to infer a detailed phylogeny. Together with comprehensive data on the parasites’ native host ranges, associations be- tween phylogenetic lineages and host specificity are tested. Key Results Within the two currently recognized species of O. sect. Gymnocaulis, seven strongly supported clades were found. While commonly sympatric, members of these clades each had unique host associations. Strong support for cryptic host-specific diversity was also found in sect. Nothaphyllon, while other taxonomic species were at University of California, Berkeley on August 28, 2016 well supported. We also find strong evidence for multiple amphitropical dispersals from central North America into South America. Conclusions Host-switching is an important driver of diversification in western hemisphere broomrapes, where host specificity has been grossly underestimated. More broadly, host specificity and host-switching probably play fundamental roles in the speciation of parasitic plants. Key words: Amphitropical disjunction, cryptic speciation, holoparasite, host-switching, Orobanche, Orobanchaceae, parasite, phylogeny. INTRODUCTION clades (Schneeweiss et al., 2004a; Park et al., 2008; McNeal et al.,2013; Schneeweiss, 2013), and the significant economic Parasitism is a highly successful life strategy that has evolved damage caused by several Eurasian species to major agricul- independently >60 times among animals, at least 12 times tural systems worldwide (Joel et al.,2013). among angiosperms, and repeatedly in protozoans and prokary- Despite the interest in this group, relatively little is known otes (Poulin and Morand, 2000; Westwood et al.,2010). While about the role of host specificity in broomrape diversification. the evolutionary significance of host–parasite associations has Understanding host specificity of parasites is predicated on a long been recognized (Kellogg, 1913), the main evolutionary comprehensive understanding of lineage boundaries in the host mechanisms involved in the generation and maintenance of (e.g. Labrousse et al.,2001; Timko et al.,2012)and,moreim- such ecological and phylogenetic diversity are still poorly un- portantly for Orobanche, the parasite. That is, failure to recog- derstood, especially among parasitic flowering plants (de nize evolutionary diversity in the parasite results in an Vienne et al., 2013; Joel et al.,2013). overestimation of host breadth and may limit the ability to un- The parasitic broomrapes, Orobanche sensu lato (s.l.)[alter- derstand the evolutionary processes responsible for speciation natively circumscribed as the genera Aphyllon and Myzorrhiza in plant parasites (Refre´gier et al., 2008). Therefore, it is impor- in the New World, and Boulardia, Orobanche sensu stricto tant to distinguish true host generalists from taxa that comprise (s.s.)andPhelipanche in the Old World: Schneeweiss (2013)], several cryptic lineages artificially united on the basis of super- have attracted significant attention as an important system for ficial similarity but distinguished genetically and ecologically. understanding the evolutionary consequences of parasitism. Host specificity to the family or genus level has been cited as a This attention is in part a result of their extensive worldwide di- key factor in the differentiation and genetic isolation of three versity (at least 170 species; Ulrich et al., 1995), a detailed and subspecies of the European O. minor (Thorogood et al.,2008, well-supported understanding of their placement within the 2009), but this has not been broadly tested across other family Orobanchaceae as well as the relationships among major Orobanche lineages. Several recently described species of VC The Author 2016. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: [email protected] Page 2 of 11 Schneider et al. — Evolution of New World Orobanche Marie-Victorin 27906 WIS282511 nrDNA Talbot 160 ALAv122774 Lipkin 04-324 ALAv156078 (ITS + ETS) Bouchard 86-94 MT26938 1 Wood s.n. MO6010393 O. uniflora subsp. uniflora Sheviak 7072 UC2046154 Melburn s.n. V101353 Lomer 7268 UBC234660 (Astereae + Rudbeckia) Kucyniak 76 WIS282505 Henson 1499 WIS282510 dePamphilis 94-15 PENN 1 Cochrane 255 WIS282508 Anderson 2267 MIN Thorne 4794 NY 0·99 Oswald 5615 UC1609174 Polster s.n. V93858 Antennaria 0·98 Ahart 10765 CHSC87344 Cowell 07-58 YM216905 + Senecio 1 1 Lackschewitz 4307 NY 1 Heckard 3286 JEPS70862 Saxifragales 1 Colwell 04-63 YM118104 O. uniflora subsp. 1 Colwell 96-WA-LC WTU344845 Fiely 91 WS285758 occidentalis Duthie s.n. WIS282512 1 Ahart 9846 CHSC82361 1 Ahart 7286 CHSC63258 Ahart 1984 CAS853689 Apioideae Colwell 14-11 JEPS 126167 Chisaki 661 WIS282509 Hitchcock 18630 WS185460 0·96 Artemisia 1 Halse 908 ARIZ187532 Lackschewitz 6619 WTU272369 Bohrer1684 ARIZ189922 1 Merner s.n. WIS282500 0·98 Keith s.n. WIS282501 0·99 Batten 78-279 ALAv85763 1 0·99 Colwell 95-CO-TFS WTU344763 Downloaded from Orobanche sect. Bell 159 SD136414 1 Banks 689 SD137701 Gymnocaulis 1 Harvey s.n. UC 0.94 Cox 188 CHSC12931 Galium 1 Colwell 07-53 YM 0·97 Colwell 10-107 YM 1 0·98 Colwell 04-83 YM118109 Yatskievych 82-196 ARIZ236136 O. fasciculata Boyd 9673 RSA599655 Egger 1295 WTU Ahart 3393 CHSC44286 Eriogonum, 1 Colwell04-54 YM117945 Colwell 04-03 YM118118 Eriodictyon, Howell 51680 CAS641193 1 Colwell 02-44 YELLO Eriophyllum, http://aob.oxfordjournals.org/ Colwell 02-09 WTU351387 Schneider 920 JEPS122893 + Phacelia Schneider 468 JEPS 0.98 Colwell 01-95 WTU351381 Colwell 99-CA-RCRS WTU344759 0·93 Mistretta 1867 RSA641370 Mistretta 1866 RSA641369 subsp. valida 1 Colwell 99-73 WTU344847 O. valida (Garrya) Rugyt 1823 JEPS110567 1 Colwell 02-04 WTU351386 subsp. howellii 0·93 Santana 5977 WIS282502 O. dugesii Vandevender 95-1215 ARIZ321887 Collins 2027 (subsp.palmeri) O. cooperi 0·95 1 1 Colwell 02-06 WTU351385 Colwell CA-SN WTU344843 (Heliantheae) 1 Colwell 01-01 WTU344743 Schneider 936 JEPS122909 Hammond 10858 ASU60715 0·99 1 1 Collins 1541 WIS282497 Colwell 03-08 JEPS126150 O. bulbosa (Adenostoma) Orobanche 1 Colwell 99-01 WTU344744 Colwell (5-July-2009) 1 Hamilton s.n. JEPS126153 at University of California, Berkeley on August 28, 2016 sect. Myzorrhiza Colwell 05-413 JEPS126144 O. parishii subsp. parishii (Artemisia) 1 1 Colwell 95-CO-DD WTU344764 Colwell 01-114 WTU351399 O. ludoviciana (Artemisia) 1 Collins 2035 MO6012141 (subsp. mutabilis) 0·97 Leidolf 2385 WTU344762 O. corymbosa (Artemisia) Colwell 99-08 WTU344753 Taylor 18332 WTU351384 Taylor 18333 WTU351383 O. parishii subsp. parishii Colwell 03-53 JEPS126149 1 Colwell 07-72 JEPS126137 (Asteroideae) Colwell 05-414 JEPS126143 0·93 Colwell 14-26 JEPS126165 0·98 Colwell 06-421 JEPS126163 Colwell 05-212 JEPS126139 O. corymbosa (Artemisia) 0·99 Holmgren 1402 WTU224934 0·97 Colwell 14-25 YM subsp. grayana (Astereae) Colwell 05-259 JEPS Colwell 03-57 WTU O. californica 1 AC 97-CA-BLO WTU344755 1 AC 99-77 WTU344846 subsp. californica (Grindelia) AC 96-WA-DPSP O. californica AC 99-76 WTU344749 0·93 Stoughton 583 RSA767875 subsp. parishii 1 Colwell (7-May-2006) JEPS O. parishii 1 Sproul & Wolf s.n. JEPS subsp. brachyloba 0·98 Colwell JEPS126159 0·95 Colwell 07-25 JEPS126141 subsp. parishii Colwell 01-104 WTU351396 subsp. jepsonii 1 Colwell 99-75 WTU344745 Colwell JEPS126158 1 Colwell 99-02 WTU344758 subsp. feudgei (Artemisia) O. californica Colwell 05-33 JEPS126147 1 Colwell JEPS126157 complex 1 Colwell 02-57 WTU351404 1 Colwell 01-116 WTU351394 Colwell 01-106 WTU351393 O. vallicola (Sambucus) 1 Prothero s.n. JEPS126154 Colwell JEPS 126162 JEPS 1 Colwell 02-52 WTU351391 Colwell 00-44 WTU344754 subsp. grandis (Lessingia) Colwell JEPS126164 Colwell 05-101 JEPS126146 Gowen s.n. JEPS126142 subsp. jepsonii Colwell 08-599 JEPS126151 subsp. grandis (Lessingia) Taylor 18568 JEPS100408 Taylor 18566 JEPS100409 subsp. condensa (Heterotheca) Taylor 18565 JEPS100410 Colwell 04-314 0·98 Colwell 02-51
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