Refugia and Geographic Barriers of Populations of the Desert Poppy, Hunnemannia Fumariifolia (Papaveraceae)
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Org Divers Evol (2012) 12:133–143 DOI 10.1007/s13127-012-0089-z ORIGINAL ARTICLE Refugia and geographic barriers of populations of the desert poppy, Hunnemannia fumariifolia (Papaveraceae) Eduardo Ruiz-Sanchez & Flor Rodriguez-Gomez & Victoria Sosa Received: 18 July 2011 /Accepted: 22 March 2012 /Published online: 15 April 2012 # Gesellschaft für Biologische Systematik 2012 Abstract Phylogeographic data and divergence estimation Oriental and the Trans-Mexican Volcanic Belt. Furthermore, times as well as current and past ecological niche modeling all of these processes may have resulted in the patchy for the Mexican tulip poppy, Hunnemannia fumariifolia distribution of suitable microhabitats for H. fumariifolia in Sweet, were combined in order to understand its biogeo- its geographical range. Ecological niche models constructed graphic history. Divergence times were estimated to deter- using the MIROC3 model indicated that populations did not mine if divergence occurred during the Pleistocene. move to the north but rather that they had suitable ecological Ecological niche modelling was used to determine if the last habitats in the Chihuahuan Desert, which harbored Pinus- glacial maximum (LGM) was responsible for the southward Juniperus forests during that period. movement of poppy populations into the Tehuacán-Cuicat- lán Valley. Analyses were performed to detect any geo- Keywords Climate change . Ecological niche models . Last graphical barriers that might have caused genetic glacial maximum . Chihuahuan Desert . Sierra Madre discontinuities among populations across the entire range Oriental . Trans-Mexican Volcanic Belt. of distribution. Current and Pleistocene ecological niche models were created for H. fumariifolia using eight envi- ronmental variables derived from temperature and precipi- Introduction tation. The evidence shows that divergence of the three main clades in H. fumariifolia occurred from the Early Pleisto- An increasing number of biogeographic studies dealing with cene to Mid-Miocene. It was also found that gene flow a diverse array of species from North America have identi- between the populations of H. fumariifolia could have been fied areas that served as refugia during the last glacial limited by the LGM, by climate change during the Quater- maximum (LGM) in the Late Pleistocene. Studies combine nary, and by the complex topography of the Sierra Madre ecological niche modelling and molecular evidence to esti- mate the time of origin, divergence of populations, abiotic E. Ruiz-Sanchez (*) factors influencing adaptation to habitats and the historical University of California, Berkeley, Plant and Microbial Biology, events that have had an effect on the evolutionary processes 431 Koshland Hall, of these taxa (e.g., Riddle et al. 2000; Carstens and Richards Berkeley, CA 94270, USA e-mail: [email protected] 2007; Castoe et al. 2007; McGuire et al. 2007; Knowles et : al. 2007; Waltari et al. 2007; Morris et al. 2008, 2010; F. Rodriguez-Gomez V. Sosa Cavender-Bares et al. 2011; Chan et al. 2011; Cosacov et Instituto de Ecología, A. C., Biología Evolutiva, al. 2010; Désamoré et al. 2011; Ornelas et al. 2010; Reber- Apartado Postal 63, 91000, Xalapa, Veracruz, México nig et al. 2010a). The utilization of palaeoclimatic models and ecological Present Address: niche models projected onto historical landscapes provides a E. Ruiz-Sanchez spatial context for phylogeographic analyses (Carstens and Instituto de Ecología, A. C., Centro Regional de Bajío, Av. Lázaro Cárdenas 253, Richards 2007; Waltari et al. 2007). These tools have been 61600, Pátzcuaro, Michoacán, México used widely to identify refugia during the Late Pleistocene 134 E. Ruiz-Sanchez et al. LGM (Hugall et al. 2002; Carstens and Richards 2007; causing vicariance events that separated, for example, her- Marske et al. 2011). Neogene vicariance, due largely to petofauna, rodents and some plant populations from both orogenesis, and Quaternary climate change have been postu- deserts (Riddle et al. 2000; Jaeger et al. 2005; Riddle and lated as drivers of evolutionary diversification in western North Hafner 2006; Castoe et al. 2007; Leaché and Mulcahy 2007; America (Riddle and Hafner 2006) and Mexico (Bryson et al. Bryson et al. 2010a; Rebernig et al. 2010a). The Chihua- 2010b). huan Desert also acted as a barrier between the Sierra Madre To understand the biogeographic history of the Mexican Occidental and Oriental for some gymnosperms, such as tulip poppy Hunnemannia fumariifolia, we combined diver- Pinus (Moreno-Letelier and Piñero 2009). gence time estimation and palaeoclimatic models to inves- The distribution of the Mexican tulip poppy is complex tigate if Neogene orogenesis and Quaternary climatic due to the presence of three mountain ranges: the Trans- change has influenced the distribution patterns of popula- Mexican Volcanic Belt in the south, the Sierra Madre Occi- tions of the Mexican tulip poppy. Our previous phylogeo- dental to the northwest and the Sierra Madre Oriental in graphic study found that allopatric fragmentation had an north-eastern Mexico. In the middle of these mountains, the effect on genetic divergence in populations of the tulip Chihuahuan Desert is located on the Mexican Plateau. The poppy in the Sierra Madre Oriental, and that this divergence Sierra Madre Oriental has the most complicated geological may be a reflection of the complex geology of the area over history of the three formations, originating in the Laramide which this species is distributed (Sosa et al. 2009). More- formation during the Late Cretaceous to the Palaeogene over, our results suggested that the areas located in the north (80–55 Ma). This formation resulted from an orogenic event of the Sierra Madre Oriental acted as post-glacial refugia for that gave rise to the Rocky Mountain fold, the thrust belt in some populations of H. fumariifolia (Sosa et al. 2009). Canada, the Sierra Madre Oriental fold and the thrust belt in However, divergence time was not estimated for popula- Mexico (English et al. 2003). Erosion in the foothills of this tions, nor were further analyses conducted to confirm these mountain range occurred during the Palaeogene-Eocene and refugia or to discover the geographic barriers that prevented subsequently either during the Oligocene or the Neogene gene flow. (Roure et al. 2009). In contrast, the Sierra Madre Occidental The tulip poppy is an herbaceous perennial, growing in resulted from volcano-tectonic events that occurred after the xerophytic habitats at middle elevations in Mexico. In the end of the Laramide orogeny and before the episode peaks north, populations are distributed in the Chihuahuan Desert of the Sierra Madre Occidental volcanic events in the Oli- and the Sierra Madre Oriental and, crossing the Trans- gocene. The volcano-tectonic peaks occurred in three main Mexican Volcanic Belt, there are populations in the south, episodes from the mid-late Oligocene to the early Miocene, in the Tehuacán-Cuicatlán Valley (Sosa et al. 2009). Hun- at about 32–30 Ma, 30–28 Ma and 26–25 Ma (Tristán- nemannia forms part of a North American clade in the González et al. 2009). The western area of the Trans- Papaveraceae, together with Eschscholzia and Dendrome- Mexican Volcanic Belt originated during the Miocene and con (Hoot et al. 1997). the eastern area during the Holocene (Ferrari et al. 2000; An analysis of the biogeographic history of the populations García-Polomo et al. 2002). Palaeorecords from the Mio- of the Mexican tulip poppy may help to understand past cene and Pliocene at the end of the Tertiary (2–20 Ma) changes in plant distribution in the deserts of Mexico. It has indicate that plant communities reached elevated complexity been suggested that the habitats of the western highlands of the at that time, reflecting a warmer, more humid, and relatively Sierra Madre Oriental and the Chihuahuan Desert fluctuated stable climate compared to that of the Quaternary (Tausch et dramatically during the Pleistocene, and that this has resulted al. 1993). Furthermore, it has been postulated that the oro- in the cyclical downward displacement and retraction of the genesis that occurred from the Palaeogene to the Neogene pine-oak-juniper forests (Van Devender 1990; Metcalfe et al. and the Quaternary climate change were the drivers of plant 2000; Metcalfe 2006). As a result of forest shifts, populations diversification in North America (Bryson et al., 2010a). expanded their range during glacial periods and remained Our study focuses on several aspects of the evolutionary isolated in refugia at high elevations during interglacial peri- history of Hunnemannia fumariifolia populations: (1) esti- ods. Moreover, these events caused subsequent postglacial mating the time of divergence of its populations to deter- fragmentation that prevented gene flow (Bryson et al. 2010a). mine if divergence occurred during the Pleistocene; (2) During the Early Pliocene the Chihuahuan Desert, along establishing whether the LGM was responsible for the with the other North American deserts, attained its maxi- southward movement of populations into the Tehuacán- mum area but it decreased during the moist Late Pliocene Cuicatlán Valley; (3) detecting the geographical barriers that and during the Pleistocene pluvial intervals (Riddle and caused genetic discontinuities among populations across Hafner 2006). As a result of the uplift of the Sierra Madre this species’ entire range of distribution; and (4) identifying Occidental and the Mexican Plateau, the Chihuahuan