Andrea T. Kramer 2,3,4,5 , Jeremie B. Fant 3 , and Mary V. Ashley 4
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American Journal of Botany 98(1): 109–121. 2011. I NFLUENCES OF LANDSCAPE AND POLLINATORS ON POPULATION GENETIC STRUCTURE: EXAMPLES FROM THREE PENSTEMON (PLANTAGINACEAE) SPECIES IN THE GREAT BASIN 1 Andrea T. Kramer 2,3,4,5 , Jeremie B. Fant 3 , and Mary V. Ashley 4 2 Botanic Gardens Conservation International (U.S.), 1000 Lake Cook Road, Glencoe, Illinois 60022 USA; 3 Chicago Botanic Garden, 1000 Lake Cook Road, Glencoe, Illinois 60022 USA; and 4 University of Illinois at Chicago, 845 West Taylor Street, M/C 066, Chicago, Illinois 60607 USA • Premise of the study : Despite rapid growth in the fi eld of landscape genetics, our understanding of how landscape features in- teract with life history traits to infl uence population genetic structure in plant species remains limited. Here, we identify popula- tion genetic divergence in three species of Penstemon (Plantaginaceae) similarly distributed throughout the Great Basin region of the western United States but with different pollination syndromes (bee and hummingbird). The Great Basin ’ s mountainous landscape provides an ideal setting to compare the interaction of landscape and dispersal ability in isolating populations of dif- ferent species. • Methods : We used eight highly polymorphic microsatellite loci to identify neutral population genetic structure between popula- tions within and among mountain ranges for eight populations of P. deustus , 10 populations of P. pachyphyllus , and 10 popula- tions of P. rostrifl orus . We applied traditional population genetics approaches as well as spatial and landscape genetics approaches to infer genetic structure and discontinuities among populations. • Key results : A ll three species had signifi cant genetic structure and exhibited isolation by distance, ranging from high structure and low inferred gene fl ow in the bee-pollinated species P. deustus (F ST = 0.1330, R ST = 0.4076, seven genetic clusters identi- fi ed) and P. pachyphyllus ( F ST = 0.1896, RST = 0.2531, four genetic clusters identifi ed) to much lower structure and higher in- ferred gene fl ow in the hummingbird-pollinated P. rostrifl orus ( FST = 0.0638, RST = 0.1116, three genetic clusters identifi ed). • Conclusions : These three Penstemon species have signifi cant yet strikingly different patterns of population genetic structure, fi ndings consistent with different interactions between landscape features and the dispersal capabilities of their pollinators. Key words: gene fl ow; landscape genetics; microsatellite; Penstemon ; pollination syndrome; population genetic structure. Landscape features interact with life history traits to either Eucalyptus globulus ( Mimura et al., 2009 ), loss of habitat con- enhance or truncate gene fl ow in ways that are not always pre- nectivity unexpectedly enhanced gene fl ow, because primary dictable. The pattern and degree of population divergence will pollinators traveled greater distances between fragmented habi- depend largely on realized gene fl ow ( Slatkin, 1985 ), which in tats. Signifi cant differences in gene fl ow, and corresponding plants is determined by the composition, confi guration, and ma- effects on genetic divergence, can therefore exist among popu- trix quality of the landscapes they inhabit ( Manel et al., 2003 ; lations of the same species occupying different landscapes as Storfer et al., 2007 ; Holderegger and Wagner, 2008 ), as well as well as among different species occupying the same landscape. life history traits such as pollination system and dispersal sys- For most species, the interacting effects of landscape features tem ( Hamrick and Godt, 1996 ; Richards, 1997 ; Duminil et al., and life history traits on population genetic structure are poorly 2007 ). In animal-pollinated plants, landscape connectivity and understood, but the growing fi eld of landscape genetics is be- pollinator movement can affect population genetic structure in ginning to address this gap ( Storfer et al., 2010 ). unpredictable ways. For example, in two herbaceous species, The use of neutral genetic markers and traditional estimates Lantana camara (butterfl y pollinated) and Rudbeckia hirta (hy- of genetic structure like FST ( Weir and Cockerham, 1984 ) and menoptera pollinated), greater habitat connectivity predictably Nei ’ s genetic distance ( Nei, 1978 ) provide insight into popula- enhanced gene fl ow by facilitating greater pollinator movement tion genetic divergence, as do more recent Bayesian clustering among populations, decreasing population genetic divergence methods, which do not require a priori assignment of individu- ( Townsend and Levey, 2005 ). However, in the tropical forest als to populations and thus allow cryptic population genetic tree Dinizia excelsa ( Dick et al., 2003 ) and temperate forest tree structure to be identifi ed ( Pritchard et al., 2000 ). Genetic dis- tance between populations can be graphically represented via 1 Manuscript received 24 June 2010; revision accepted 22 November 2010. hierarchical genetic clustering methods such as UPGMA The authors thank K. Havens and P. Olwell for project support, and ( Sneath and Sokal, 1973 ), or it can be combined with geo- C. Newton, R. Tonietto, C. Flower, L. Jefferson, S. Karumuthil-Melethil, graphic distance information to detect patterns of isolation by E. Lukina, E. Sirkin, and J. Keller for fi eld and laboratory assistance. They distance. In landscapes where topographic features such as also thank P. Wilson and an anonymous reviewer for comments on an mountain ranges and arid valleys likely present obstacles to earlier version of this manuscript. This research was supported by the gene fl ow even for neighboring populations, newly developed Bureau of Land Management, Department of the Interior (Assistance methods allow genetic discontinuities between adjacent popu- Agreement PAA-01 – 7035), and an EPA STAR Fellowship to A.T.K. 5 Author for correspondence (e-mail: [email protected]) lations to be identifi ed (e.g., BARRIER software, Manni et al., 2004 ). Inference of gene fl ow patterns from population struc- doi:10.3732/ajb.1000229 ture can be further enhanced by combining molecular maker American Journal of Botany 98(1): 109–121, 2011; http://www.amjbot.org/ © 2011 Botanical Society of America 109 110 American Journal of Botany [Vol. 98 data directly with information on geographic landscape features Here, we focus on three Penstemon species that are similarly ( Manel et al., 2003 ; Holderegger et al., 2006 ; Storfer et al., distributed throughout the Great Basin ’ s mountainous land- 2007 ) and new statistical methods in spatial genetics ( Guillot scape and ask how landscape features affect their population et al., 2009 ). Interpreting genetic discontinuities in the context genetic structure. We use microsatellite markers and multiple of landscape features provides a powerful approach for under- analyses to identify population genetic differentiation in these standing the interaction of plant dispersal systems, landscape, species and to better understand how this structure relates to and microevolutionary processes, yielding insights relevant to landscape features. Because the species chosen for study have evolutionary biology ( Kay and Sargent, 2009 ). different pollination syndromes but otherwise similar life his- Genetically isolated populations may follow different evolu- tory characteristics, we also identify how the population genetic tionary trajectories because of a combination of mutation, ge- structure of each species may be differently affected by the in- netic drift, and/or natural selection. Extreme examples come teraction of landscape features with characteristics related to from high-elevation mountaintops like the Andes ( Hughes and their dispersal ability. We expect that genetic divergence will Eastwood, 2006 ), rock outcrop “ inselbergs ” ( Barbara et al., be greater among mountain ranges than within mountain ranges 2007 ), and the edaphically diverse habitat of southern Africa ’ s for all species but that the degree and structure of population Karoo region ( Ellis et al., 2006 ). With more than 100 separate genetic differentiation may vary for species with different pri- mountain ranges isolated by arid basins, the Great Basin region mary pollinators. Given previous fi ndings for greater long-dis- of the western United States provides the opportunity to deter- tance foraging in hummingbirds vs. bees, we expect that the mine how a complex topography infl uences gene fl ow in spe- hummingbird-pollinated species will have lower population ge- cies with different dispersal capabilities. Previous studies on netic divergence than the bee-pollinated species. plants distributed throughout the region have shown that coni- fer species that rely on wind for pollen movement and birds for seed dispersal display little population divergence ( Johnson, MATERIALS AND METHODS 1975 ; Wells, 1983 ; Hamrick and Godt, 1996 ; Jorgensen et al., 2002 ), whereas populations of terrestrial animals are more ge- Study species— This study focuses on three species: Penstemon deustus netically isolated by the regions ’ landscape ( Floyd et al., 2005 ). Douglas ex Lindl. var. pedicellatus M. E. Jones, P. pachyphyllus A. Gray ex For animal-pollinated plants, pollinator movement is likely af- Rydb. var. congestus (M. E. Jones) N. H. Holmgren, and P. rostrifl orus Kel- fected by the region ’ s steep elevational gradients, arid valleys, logg. All three species are considered common and widespread throughout sagebrush – steppe habitat in the Great Basin ( Kartesz, 1999 ). This habitat