A FRAMEWORK FOR COMMUNITY AND ECOSYSTEM GENETICS: FROM GENES TO ECOSYSTEMS

1. A FRAMEWORK FOR COMMUNITY AND ECOSYSTEM GENETICS: FROM GENES TO ECOSYSTEMS Photo credits: Tom Whitham & Carri LeRoy • Our faculty are involved with the new IGERT program at NAU to train graduate students in “Integrative Bioscience: Genes to Environment”. Photo credits: Dylan Fischer • Undergraduates at Evergreen State College trained in a 2-week Field Ecology program at common garden sites in Arizona & Utah. Photo credit: Gery Allan Photo credit: zsuzsi Kovacs 4. Conservation Implications Because individual plant genotypes support different community and ecosystem phenotypes and these phenotypes are heritable, the genetic diversity in a foundation species affects the diversity of the dependent community in two ways. First, genetically similar plants support similar communities. The left panel shows that the genetic differences among individual trees based on molecular markers are strongly associated with differences in the arthropod communities they support both within a common garden and among trees in the wild. Second, based on genetic similarity, increased genetic diversity within the plant population is positively correlated with increased species diversity of the dependent community. The right panel B shows that genetic variation in individual poplar stands accounts for nearly 60% of the variation in an arthropod community of 207 species. 1. The Concept of Community& Ecosystem Phenotypes PI - Tom Whitham (Thomas.Whitham@nau.edu), Northern Arizona Univ. (Lead Institution); NAU Co-PIs - Steve Shuster, Catherine Gehring, Gery Allan, Jane Marks, Steve Hart, & Randy Bangert; Rick Lindroth & Stuart Wooley, Univ. Wisconsin; Stephen DiFazio, West Virginia Univ.; Brad Potts, Univ. Tasmania, Australia; Carri LeRoy & Dylan Fischer, Evergreen State College, Jen Schweitzer & Joe Bailey, Univ. of Tennessee; Eric Lonsdorf, Lincoln Park Zoo, Chicago. Just as the genotype may have a ‘traditional’ phenotype that is expressed within the individual and its population, gene expression that leads to interactions with other species extends to levels above the population to produce community and ecosystem phenotypes (all illustrations from Nature Reviews Genetics 2006, in press). Abstract. Heritable traits in a single species can affect an entire ecosystem. Recent studies show that such traits in a common tree have predictable effects on community structure and ecosystem processes. Because these ’community and ecosystem phenotypes’ have a genetic basis and are heritable, we can begin to apply the principles of population and quantitative genetics to place the study of complex communities and ecosystems within an evolutionary framework. This framework may allow us to understand the genetic basis of ecosystem processes, and the impacts such phenomena as climate change and introduced transgenics may have on entire communities. 2. Demonstrating Community & Ecosystem Phenotypes Using experimental crosses of Populus angustifolia x P. fremontii, we found that a single QTL (Quantitative Trait Locus) is significantly correlated with the phenotypic variation in condensed tannins among cross types (Fig. a). These compounds have been extensively studied and are well known for their generally inhibitory effects on diverse organisms from microbes to vertebrates. The variation in condensed tannins is associated with different community phenotypes of terrestrial arthropods living in tree canopies (Fig. b), endophytic fungi inhabiting tree bark (Fig. c), and aquatic macroinvertebrates feeding on the leaves that fall into an adjacent stream (Fig. d). Similarly, we found significant ecosystem phenotypes; the effects of condensed tannins explained 65% of the variation in net nitrogen mineralization in the soil (Fig. e) and 97% of the variation in decomposition of leaves in the stream (Fig. f). 3. Heritability of Community Phenotypes - Genetic Variation Within Tree Species Structures Arthropod Communities When species comprising ecological communities are summarized using a multivariate statistical method (non-metric multidimensional scaling; NMDS), the resulting univariate scores can be analyzed using standard techniques for estimating the heritability of quantitative traits. Our estimates of the broad-sense community heritability (H2C) of arthropod communities on known genotypes of cottonwood trees in common gardens have explained 56-63% of the total variation in community phenotype. Furthermore, genetic variation within, rather than between, individual tree species structures the dependent arthropod community in the cottonwood system. Line cross and joint scaling analyses of communities on Populus angustifolia, P. fremontii, their F1s and their backcross hybrids could not reject the simplest additive model (χ2 = 1.68, df = 2, p = 0.43) indicating non-significant additive and dominant effects among parental and hybrid lines. Yet broad-sense heritability estimates for communities within each parental type (P. fremontii H2C = 0.65; P. angustifolia H2C = 0.60), and on backcross hybrids (H2C = 0.80) were all significant; only H2C on F1 hybrids was not. Larger, filled circles represent adjusted means of the arthropod community for each cross type ±S.E. from a nested ANOVA. Replicated clones of the same genotype are indicated by the same symbol within each of the four cross types. Different symbols within each of the four cross types indicate different genotypes; similar symbols in different cross types do not represent similar genotypes. 5. Training & Outreach • EnGGEN: The Environmental Genetics & Genomics facility was independently established in 2003 with NSF funding and is being used to train graduate and undergraduate students conducting FIBR research. Photo credit: Carri LeRoy Photo credit: Carri LeRoy • A 40-acre common garden planted in collaboration with the Bureau of Reclamation, USFW & at Cibola National Wildlife Refuge in 2005 involved 17 graduate students and 5 undergraduates. • FIBR PhD students include Native American and Hispanic minorities. • FIBR is now linked to an REU Site at NAU in Behavioral and Conservation Sciences. • 25 Selected Publications Since 2004 • Whitham, T.G, J.K. Bailey, J.A. Schweitzer, S.M. Shuster, R.K. Bangert, C.J. LeRoy, E. Lonsdorf, G.J. Allan, S.P. DiFazio, B.M. Potts, D.G. Fischer, C.A. Gehring, R.L. Lindroth, J. Marks, S.C. Hart, G.M. Wimp, and S.C. Wooley. 2006. A framework for community and ecosystem genetics: From genes to ecosystems. NATURE REVIEWS GENETICS (in press). • Chapman, S.C., J.A. Schweitzer and T.G. Whitham. Herbivory differentially alters plant litter dynamics of evergreen and deciduous trees. OIKOS (in press). • Rehill, B., T.G. Whitham, G.D. Martinsen, J.A. Schweitzer, J.K. Bailey, and R.L. Lindroth. Developmental trajectories in cottonwood phytochemistry. JOURNAL OF CHEMICAL ECOLOGY (in press). • Fischer, D.G., S.C. Hart, B.J. Rehill, R.L. Lindroth, P. Keim, and T.G. Whitham. Do high tannin leaves require more roots? OECOLOGIA (in press). • Gehring, C.A., R.C. Mueller, and T.G. Whitham. 2006. Environmental and genetic effects on the formation of ectomycorrhizal and arbuscular mycorrhizal associations in cottonwoods. OECOLOGIA (in press). • Gitlin, A., C.M. Stultz, M.A. Bowker, S. Stumpf, K. Ecton, K. Kennedy, A. Munoz, J.K. Bailey, and T.G. Whitham. 2006. Mortality gradients within and among dominant plant populations as barometers of ecosystem change during extreme drought. CONSERVATION BIOLOGY (in press). • Bailey, J.K., S.C. Wooley, R.L. Lindroth, and T.G. Whitham. 2006. Importance of species interactions to community heritability: A genetic basis to trophic-level interactions. ECOLOGY LETTERS 9:78-85. • Shuster, S.M., E.V. Lonsdorf, G.M. Wimp, J.K. Bailey, and, T.G. Whitham. 2006. Community heritability measures the evolutionary consequences of indirect genetic effects on community structure. EVOLUTION 60(5):991-1003. • Bailey, J.K., and T.G. Whitham. 2006. Interactions between cottonwood and beavers positively affect sawfly abundance. ECOLOGICAL ENTOMOLOGY (in press). • Bangert, R.K., R.J. Turek, B. Rehill, G.J. Allan, G.M. Wimp, J.A. Schweitzer, J.K. Bailey, G.D. Martinsen, P. Keim, R.L. Lindroth, and T.G. Whitham. 2006. A genetic similarity rule determines arthropod community structure. MOLECULAR ECOLOGY 15:1379-1392. • LeRoy, C.J., T.G. Whitham, P. Keim, and J.C. Marks. 2006. Plant genes link forests and streams. ECOLOGY 87:255-261. • Loeser, M.R., B.H. McRae, M.M. Howe, and T.G. Whitham. 2006. Litter hovels as havens for riparian spiders in an unregulated river. WETLANDS 26:13-19. • Schweitzer, J.A., J.K. Bailey, S.C. Hart, and T.G. Whitham. 2005. Nonadditive effects of mixing cottonwood genotype on litter decomposition and nutrient dynamics. ECOLOGY 86:2834-2840. • Bailey, J.K., R. Deckert, J.A. Schweitzer, B.J. Rehill, R.L. Lindroth, C.A. Gehring, and T.G. Whitham. 2005. Host plant genetics affect hidden ecological players: Links among Populus, condensed tannins and fungal endophyte infection. CANADIAN JOURNAL OF BOTANY 83:356- 361. • Whitham, T.G., E. Lonsdorf, J.A. Schweitzer, J.K. Bailey, D.G. Fischer, S.M. Shuster, R.L. Lindroth, S.C. Hart, G.J. Allan, C.A. Gehring, P. Keim, B.M. Potts, J. Marks, B.J. Rehill, S.P. DiFazio, C.J. LeRoy, G.M. Wimp, and S. Woolbright. 2005. “All effects of a gene on the world”: Extended phenotypes, feedbacks and multi-level selection. ECOSCIENCE 12:5-7. • We have restored over 75 acres of critical riparian habitat jointly with the BOR, Utah DNR, USFW, Ogden Nature Center, Swaner Nature Reserve and the Arboretum at Flagstaff. • Schweitzer, J.A., J.K. Bailey, S.C. Hart, G.M. Wimp, S.K. Chapman, and T.G. Whitham. 2005. The interaction of plant genotype and herbivory decelerate leaf litter decomposition and alter nutrient dynamics. OIKOS 110:133-145. • Rehill, B., A. Clauss, L. Wieczorek, T.G. Whitham, and R.L. Lindroth. 2005. Foliar phenolic glycosides from Populus fremontii, Populus angustifolia, and their hybrids. BIOCHEMICAL SYSTEMATICS AND ECOLOGY 33:125–131. • Wimp, G.M., G.D. Martinsen, K.D. Floate, R.K. Bangert, and T.G. Whitham. 2005. Plant genetic determinants of arthropod community structure and diversity. EVOLUTION 59:61-69. • *Cox, G., D. Fischer, S.C. Hart, and T.G. Whitham. 2005. Nonresponse of native cottonwood trees to water additions during summer drought. WESTERN NORTH AMERICAN NATURALIST 65:175-185. • Bangert, R.K., R.J. Turek, G.D. Martinsen, G.M. Wimp, J.K. Bailey, and T.G. Whitham. 2005. Benefits of conservation of plant genetic diversity on arthropod diversity. CONSERVATION BIOLOGY 19:379-390. • Wimp, G.M., W.P. Young, S.A. Woolbright, G.D. Martinsen, P. Keim, and T.G. Whitham. 2004. Conserving plant genetic diversity for dependent animal communities. ECOLOGY LETTERS 7:776-780. • Bailey, J.K., R.K. Bangert, J.A. Schweitzer, R.T. Trotter III,S.M. Shuster, and T.G. Whitham. 2004. Fractal geometry is heritable in trees. EVOLUTION 58:2100- 2102. • Fischer, D.G., S.C. Hart, and T.G. Whitham, G.D. Martinsen, and P. Keim. 2004. Ecosystem implications of genetic variation in water-use of a dominant riparian tree. OECOLOGIA 139:288–297. • Bailey, J.K., J.A. Schweitzer, B.J. Rehill, R.L. Lindroth, G.D. Martinsen, and T.G. Whitham. 2004. Beavers as molecular geneticists: A genetic basis to the foraging of an ecosystem engineer. ECOLOGY 85:603-608. • Schweitzer, J.A., J.K. Bailey, B.J. Rehill, G.D. Martinsen, S.C. Hart, R.L. Lindroth, P. Keim, and T.G. Whitham. 2004. Genetically based trait in a dominant tree affects ecosystem processes. ECOLOGY LETTERS 7:127-134. • *indicates undergraduate as the lead author • We are involved in outreach to all ages at the Ogden Nature Center (UT), Swaner Nature Preserve (UT), the Arboretum at Flagstaff (AZ) & the Flagstaff Festival of Science.