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Amphitropical Disjunctions in New World Menthinae: Three Pliocene Dispersals to South America Following Late Miocene Dispersal to North America from the Old World1

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Amphitropical Disjunctions in New World Menthinae: Three Pliocene Dispersals to South America Following Late Miocene Dispersal to North America from the Old World1 RESEARCH ARTICLE AMERICAN JOURNAL OF BOTANY INVITED PAPER For the Special Issue: Patterns and Processes of American Amphitropical Plant Disjunctions: New Insights Amphitropical disjunctions in New World Menthinae: Three Pliocene dispersals to South America following late Miocene dispersal to North America from the Old World1 Bryan T. Drew2,5 , Sitong Liu 2 , Jose M. Bonifacino 3 , and Kenneth J. Sytsma 4 PREMISE OF THE STUDY: The subtribe Menthinae (Lamiaceae), with 35 genera and 750 species, is among the largest and most economically important subtribes within the mint family. Most genera of Menthinae are found exclusively in the New World, where the group has a virtually continuous distribu- tion ranging from temperate North America to southern South America. In this study, we explored the presence, timing, and origin of amphitropical dis- juncts within Menthinae. METHODS: Our analyses were based on a data set consisting of 89 taxa and the nuclear ribosomal DNA markers ITS and ETS. Phylogenetic relationships were determined under maximum likelihood and Bayesian criteria, divergence times were estimated with the program BEAST, and ancestral range esti- mated with BioGeoBEARS. KEY RESULTS: A North Atlantic Land Bridge migration event at about 10.6 Ma is inferred from western Eurasia to North America. New World Menthinae spread rapidly across North America, and then into Central and South America. Several of the large speciose genera are not monophyletic with nuclear rDNA, a fi nding mirrored with previous chloroplast DNA results. Three amphitropical disjunctions involving North and southern South America clades, one including a southeastern South American clade with several genera, were inferred to have occurred within the past 5 Myr. CONCLUSIONS: Although three New World Menthinae genera occur in both North and South America, none exhibit an amphitropical disjunction. However, three clades exhibit amphitropical disjunctions, all dating to the early Pliocene, and all involve jump dispersals to either southeastern or southwestern South America from southeastern North America. KEY WORDS BEAST; biogeography; BioGeoBEARS; disjunct; jump dispersal; Lamiaceae; mint family Closely related organisms that exhibit wide gaps in their ranges, between diff erent continents (intercontinental disjunctions; Raven, or taxa with disjunct distributions, have long puzzled biologists 1963 , 1972 ; Th orne, 1972 ; Tripp and McDade, 2014 ; Wen et al., ( Darwin, 1859 ; Wallace, 1880 ; Baker, 1959 ; Raven, 1972 ; Carlquist, 2016 ; Simpson et al., 2017 ). Intracontinental organismal disjunc- 1974 ; Briggs, 2009 ). Not all disjunctions are formed equally, how- tions are typically more readily explained and understood than ever. Taxa can be disjunct within relatively small political boundar- their more perplexing counterpart, intercontinental disjunctions ies such as a state, province, or country, or across larger natural ( Th orne, 1972 ; Axelrod, 1975 ; Wen, 1999 ; Givnish and Renner, landscapes such as continents (intracontinental disjunctions), or 2004 ; Wen and Ickert-Bond, 2009 ; Simpson et al., 2017 ). By under- standing plate tectonics, past sea level fl uctuations, and paleocli- 1 Manuscript received 6 June 2017; revision accepted 5 September 2017. mate regimes, some intercontinental disjunctions, such as East 2 Department of Biology, University of Nebraska-Kearney, NE Kearney 68849 USA; Asian/European/Eastern North America, are easily explained, at 3 Laboratorio de Botánica, Facultad de Agronomía, Casilla de Correos 1238, Montevideo, least in part, by ancient vicariance. Th e most challenging types of Uruguay; and disjunctions to clarify are those that are widely separated spatially, 4 Department of Botany, University of Wisconsin, Madison, Wisconsin 53706 USA 5 Author for correspondence (e-mail: bdrewfb @yahoo.com); ORCID id 0000-0001-7248-2799 occur in areas that were never in physical proximity nor bridged by https://doi.org/10.3732/ajb.1700225 a common vegetation type or climatic regime, and hence cannot be AMERICAN JOURNAL OF BOTANY 104 (11): 1695 – 1707 , 2017; http://www.amjbot.org/ © 2017 Botanical Society of America • 1695 1696 • AMERICAN JOURNAL OF BOTANY logically explained by vicariance, ancient or otherwise. Within this New World representation of Menthinae includes about 23 gen- narrower subset of disjunctions are species distributions that occur era, with three that occur in both the northern and southern hemi- in northern and southern temperate regions but bypass the tropics, spheres: Clinopodium , Cunila , and Hedeoma. Clinopodium is a known as amphitropical (and bipolar) disjunctions ( Raven, 1963 ; taxonomically challenging, nonmonophyletic assemblage of taxa Solbrig, 1972 ; Wen and Ickert-Bond, 2009 ; Donoghue, 2011 ; Baldwin ( Doroszenko, 1986 ; Cantino and Wagstaff , 1998 ; Bräuchler et al., and Wood, 2016 ; Simpson et al., 2017 ). 2010 ; Drew and Sytsma, 2011 , 2012 ) that contains about 150 spe- Th e mint family (Lamiaceae) contains over 7000 species and is cies ( Th e Plant List, 2017 ) mostly distributed across Eurasia and the diverse on six continents. Th e mints are divided into 12 subfamilies New World ( Harley et al., 2004 ). Th ere are about 70 species of New ( Li et al., 2016 ; Li and Olmstead, 2017 ), and several of these sub- World Clinopodium that range from southern Canada to southern families are further subdivided into tribes and subtribes. Th e largest Argentina. Th is group is morphologically heterogeneous and oc- mint subfamily is the Nepetoideae, which represents almost half curs in a wide variety of habitats. Cunila contains about 20 species (ca. 3400) of the species in the Lamiaceae. Although the Nepetoi- and occurs in the eastern United States (one species) from southern deae is widely distributed, the tribes and subtribes within it are of- New York to northeastern Texas, mountains of central Mexico ten confi ned to relatively narrow geographic regions (excepting to northern Central America, and southeastern South America Salvia ). For example, the subtribes Ociminae and Plectranthinae (northeastern Argentina, southeastern Brazil, southeastern Para- (tribe Ocimae) are extremely diverse in tropical Africa (and to a guay, and Uruguay). Hedeoma is composed of about 40 species lesser extent Australia) but virtually absent in the New World and and ranges from northeastern North America to southern South temperate Eurasia. Conversely, subtribe Hyptidinae (also tribe Oci- America. Formerly, the genus Hesperozygis was considered to mae) is extremely diverse in tropical and subtropical environments occur in Mexico and southeastern South America, but the Mexican in the New World, but virtually absent in the Old World. Th e sub- taxa are now treated in Poliomintha ( P. marifolia ) and Hedeoma tribe Menthinae (tribe Mentheae) is one of the few subclades within ( H. ciliolata ). the Nepetoideae (or more broadly the Lamiaceae) that is wide- Th us, the New World Menthinae has a virtually continuous distri- spread, although not especially diverse, across fi ve continents, and bution from temperate North America to southern South America. has striking amphitropical distributions. However, no study has explicitly examined the relationships of the Menthinae, with about 35 genera and 750 species ( Harley et al., three genera that occur in both North and South America nor the 2004 ; Bräuchler et al., 2010 ; Drew and Sytsma, 2012 ), is one of the temperately distributed Menthinae in a phylogenetic context. Fur- largest and most economically important subtribes within the mint thermore, no detailed, model-based biogeographic analysis has been family. Th e group contains familiar culinary spices such as oregano performed on the New World Menthinae in the context of defi ned ( Origanum vulgare ), marjoram (O. majorana ), thyme ( Th ymus ser- specific areas, both adjacent and disjunct. Here, we employ two pyllum ), peppermint and spearmint ( Mentha × piperita and M. spi- nuclear ribosomal DNA regions (internal and external transcribed cata ), and summer and winter savory (Satureja hortensis and S. spacers) to generate a phylogenetic framework of Menthinae with montana ), and various horticulturally important plants. Although which to apply model based ancestral region estimation (ARE). We most species of Menthinae with widespread culinary applications address the following questions: (1) Are there amphitropical disjunct are native to the Old World, most of the genera of Menthinae (ca. clades in New World Menthinae? (2) If so, when did these disjunc- 22/35) are found exclusively in the New World. Th ese genera have tions occur? (3) What was the directionality of movements for these radiated into a large and morphologically diverse clade of species disjunctions? (4) How did these disjunctions arise? ( Fig. 1 ). Previous studies have suggested that the New World Men- thinae radiation occurred aft er a single colonization event, but chloroplast and nuclear ribosomal DNA (nrDNA) give confl icting MATERIALS AND METHODS results as to what lineage is sister to the New World Menthinae ( Trusty et al., 2004 ; Bräuchler et al., 2010 ; Drew and Sytsma, 2012 ). Nomenclature— Taxonomic descriptions used in this paper gener- Within Menthinae, two genera, Mentha and Clinopodium , occur ally follow the species descriptions of Epling ( Epling, 1937 ; Irving, in both the Old and New World. Th e only native New World spe- 1980 ; Harley and Paucar, 2000 ), and the broad taxonomic treat- cies of Mentha is M. arvensis , which has a circumboreal
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