Whitham, T.G., C.A. Gehring, L.M. Evans, C.J. LeRoy, R.K ...jenschweitzer.com/wp-content/uploads/2010-Mol-Approaches...R.C. Barbour, D.G. Fischer, B.M. Potts, and J.K. Bailey. 2010

Whitham, T.G., C.A. Gehring, L.M. Evans, C.J. LeRoy, R.K. Bangert, J.A. Schweitzer, G.J. Allan,

R.C. Barbour, D.G. Fischer, B.M. Potts, and J.K. Bailey. 2010. A community and ecosystem

genetics approach to conservation biology and management. Pages 50-73 in Molecular Approaches

in Natural Resource Conservation and Management (A. DeWoody, J. Bickham, C. Michler, K.

Nichols, G. Rhodes and K. Woeste, eds.). Cambridge University Press.

Note: The editor would not provide final copy, so these galleys contain a few minor errors. For example,

substitute H´ in the legend of Fig. 3 and the page numbers are incorrect as a box was inserted into the

text, which doesn’t show in these galleys.

P1: ICD Trim: 7in × 10in Top: 0.375in Gutter: 1inCUUS999-03 cuus999/DeWoody ISBN: 978 0 521 51564 1 February 26, 2010 20:32

3 A community and ecosystem genetics approachto conservation biology and management

Thomas G. Whitham, Catherine A. Gehring, Luke M. Evans, Carri J. LeRoy,Randy K. Bangert, Jennifer A. Schweitzer, Gerard J. Allan, Robert C. Barbour,Dylan G. Fischer, Bradley M. Potts, and Joseph K. Bailey

INTRODUCTION

The emerging field of community and ecosystem genetics has so far focused onhow the genetic variation in one species can influence the composition of asso-ciated communities and ecosystem processes such as decomposition (see defini-tions in Table 3–1; reviews by Whitham et al. 2003, 2006; Johnson & Stinchcombe2007; Hughes et al. 2008). A key component of this approach has been an empha-sis on understanding how the genetics of foundation plant species influence amuch larger community. It is reasoned that because foundation species struc-ture their ecosystems by creating locally stable conditions and provide specificresources for diverse organisms (Dayton 1972; Ellison et al. 2005), the geneticsof these species as “community drivers” are most important to understand andmost likely to have cascading ecological and evolutionary effects throughoutan ecosystem (Whitham et al. 2006). For example, when a foundation species’genotype influences the relative fitness of other species it constitutes an indi-rect genetic interaction (Shuster et al. 2006), and when these interactions changespecies composition and abundance among individual tree genotypes, they resultin individual genotypes having distinct community and ecosystem phenotypes.Thus, in addition to an individual genotype having the “traditional” pheno-type that population geneticists typically consider as the expression of a trait atthe individual and population level, community geneticists must also considerhigher-level phenotypes at the community and ecosystem level. The predictabil-ity of phenotypes at levels higher than the population can be quantified as com-munity heritability (i.e., the tendency for related individuals to support similarcommunities of organisms and ecosystem processes; Whitham et al. 2003, 2006;Shuster et al. 2006).

Numerous studies in diverse systems demonstrate that community and ecosys-tem phenotypes exist (e.g., cottonwoods – Dickson & Whitham 1996; Whitham

We thank the NSF for an Frontiers of Integrative Biological Research grant to bring togetherdiverse scientists to help integrate and develop the emerging field of community andecosystem genetics. NSF IGERT and Science Foundation Arizona grants supported studentresearch; The Australian Research Council (grants DP0451533 and DP0773686) supportedparallel studies in Australia, and NSF grant DEB-0816675 supported climate change researchin the United States. The Ogden Nature Center, the Utah Department of Natural Resourcesand Reclamation provided lands for common gardens, restoration, and public outreach.

50


A community and ecosystem genetics approach to conservation 51

Table 3–1. Definitions of community genetics terms

Community and ecosystem genetics – The study of the genetic interactions that occur amongspecies and their abiotic environment in complex communities

Community and ecosystem phenotypes – The effects of genes at levels higher than thepopulation. These phenotypes result from interspecific indirect genetic effects, which can besummarized as a univariate trait.

Community heritability – The tendency for related individuals to support similar communitiesof organisms and ecosystem processes

Foundation species – Species that structure a community by creating locally stable conditionsfor other species, and by modulating and stabilizing fundamental ecosystem processes

Minimum viable population (MVP) – The size of a population that, with a given probability,will ensure the existence of the population for a stated period of time

Minimum viable interacting population (MVIP) – The size of a population that is required tomaintain genetic diversity at levels required by other dependent and interacting species in acommunity context

et al. 2003; Bailey et al. 2004, 2006; Fischer et al. 2004, 2006, 2007; Schweitzeret al. 2004, 2005a,b, 2008; Wimp et al. 2005, 2007; LeRoy et al. 2006, 2007;Shuster et al. 2006; aspen – Madritch et al. 2006, 2007; willows – Fritz & Price1988; Hochwender & Fritz 2004; metrosideros – Treseder & Vitousek 2001; oaks –Madritch & Hunter 2002, 2004; Tovar-Sanchez & Oyama 2006; aspen – Madritchet al. 2006, 2007; Donaldson & Lindroth 2007; seagrass – Hughes & Stachowicz2004; goldenrod – Maddox & Root 1987; Crutsinger et al. 2006; Crawford et al.2007; eucalypts – Dungey et al. 2000; Barbour et al. 2009; evening primrose –Johnson & Agrawal 2005; Johnson et al. 2006; Johnson 2008; common reed –Araki et al. 2005; birch – Silfver et al. 2007; alder – Lecerf & Chauvet 2008; grape –English-Loeb & Norton 2006; Baccharis – Rudgers & Whitney 2006). Althoughmost of the species examined in these studies are considered to be foundationspecies in their respective ecosystems, the evening primrose is a notable excep-tion. Thus, it would appear that a community genetics approach need not belimited to just foundation species.

Having demonstrated that different plant genotypes support different commu-nities, new emphasis must be placed on understanding the implications of thesefindings. For example, relatively few studies have quantified how the geneticvariation in foundation species might also affect the evolution of dependentcommunity members (e.g., review by Mopper 1996 and more recent studies onoaks – Mopper et al. 2000; goldenrod – Craig et al. 2007; cottonwood – Evans et al.2008), how the genetic variation in a foundation species in one community mightaffect another community (e.g., terrestrial affects aquatic – Driebe & Whitham2000; LeRoy et al. 2006, 2007; Lecerf & Chauvet 2008), and how a communitymight feed back to affect the survival and performance of the genotype express-ing the trait (e.g., soil microbial community impacts on a host tree; Fischer et al.2006; Schweitzer et al. 2008). These frontiers of research remain important fora community genetics approach to reach its full conceptual potential. Based onour current knowledge, however, it seems clear that this approach can offer pro-ductive insights into conservation biology and management. The remainder ofthis chapter considers the conservation implications of the existence of heritablecommunity and ecosystem phenotypes.


52 Whitham, Gehring, Evans, LeRoy, et al.

CONSERVATION IN A COMMUNITY CONTEXT

There are two main reasons to support a community genetics approach for con-servation and management. First, because all species have evolved in a commu-nity context of many interacting species and their abiotic environments, it isunrealistic to study any one species in isolation as if it had evolved in a vacuum(e.g., Thompson 2005; Wade 2007). Thus, the community context of species evo-lution is far more realistic as it considers more of the variables that are likely tohave influenced the evolution of any one species.

Second, and perhaps more important from a manager’s perspective, a com-munity approach is less likely to result in management errors. For example, asa two-way interaction, mistletoes are clearly parasites of flowering plants. Fewinteractions are just two-way interactions, however. In their studies of one-seedjuniper ( Juniperus monosperma) and its associated mistletoe (Phoradendron juniper-inum), van Ommeren and Whitham (2002) found that the berries produced byboth the juniper and the mistletoe were primarily dispersed by birds such asTownsend’s Solitaires (Myadestes townsendi). If the seeds of mistletoe attract morebirds that end up dispersing more juniper berries, then as a three-way interaction,mistletoe might be considered as a mutualist rather than a parasite. In supportof this hypothesis, they found that juniper stands with mistletoe attracted up to3 times more birds than did stands with little or no mistletoe. Most importantly,the number of juniper seedlings was more than twofold greater in stands withhigh mistletoe density compared with stands that had little or no mistletoe. Amanager would be justified in the case of a two-way interaction in removingmistletoe to promote tree performance. In the case of a three-way interaction,however, the opposite strategy might be warranted because the mistletoe bene-fits juniper recruitment by promoting avian seed dispersal. Thus, just by addingone additional species to the analysis, the fundamental relationships of juniperand mistletoe can “switch or reverse” from negative to positive, and manage-ment decisions would also shift accordingly. Because the species composing acommunity interact, the sign of the ecological interaction and the appropriatemanagement decision is dependent on the number of interacting players andtheir combined interactions.

Although the previously mentioned study demonstrates how a communityanalysis versus a population analysis can result in a qualitative change in inter-pretation that affects management decisions, it is important to know whethersuch reversals in interpretation are common enough to warrant concern. Bai-ley and Whitham (2007) reviewed 85 studies and 417 tests that varied in thenumber of factors examined in scientific studies, which included numbers ofspecies, geographic scale (e.g., local to global), and number of years of the study(Fig. 3–1). When the study included only one factor, there was no chance ofdetecting either a significant interaction or a reversal in outcome as it is beyondthe ability of the statistical approach. When two factors were included in thestudy, however, there was a 55% probability of detecting a significant interactionterm (solid bars), and this probability increased to nearly 95% when four factorswere included in the analysis. Note that such an interaction term could be justa “quantitative” change in which the sign of an interaction would still remain



# of Statistical Factors

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Figure 3–1: A survey of the literature shows that interaction effects and pattern reversals arecommon, which argues for a community approach to avoid potentially costly errors in conservationand management decisions. Solid bars show that as the number of factors in a study increases,the observed percentage of significant interaction effects also increases (i.e., both quantitativeand qualitative interactions). Open bars show that, as the number of factors in a study increases,the observed percentage of reversals also increases (i.e., a qualitative change in the sign of aninteraction). Figure from Bailey and Whitham (2007).

the same (i.e., negative remains negative, and positive remains positive). Moreimportantly, they found that, as the number of factors increased, the numberof reversals also increased such that, when the analysis included four factors,there was a nearly 80% probability that the sign of the interaction of one ormore factors reversed from negative to positive or from positive to negative.These “qualitative” changes in interpretation are the most vexing, as they havea high probability of resulting in fundamental management errors. This studyconcluded that, to avoid such errors, conservation biologists and managers needto adopt a long-term, community approach that covers a large geographic area.

Because species interact with one another (i.e., it is a multivariate world), onlyby including the major interacting species can one really understand the sign ofthe interactions. This is why a community approach is desirable and is less likelyto result in management errors that are both costly and produce unintendedeffects.

HERITABLE COMMUNITY AND ECOSYSTEM PHENOTYPES

To justify a community genetics approach it is essential to demonstrate that com-munity and ecosystem phenotypes exist and that they are heritable. Although



Figure 3–2: Community and ecosystem phenotypes of individual tree genotypes of P. angustifo-lia show broad-sense heritability (H2). Significant heritability of the canopy arthropod community,soil microbial community, trophic interactions between birds and insects, and soil nutrient poolsdemonstrate how trait variation in a foundation tree can structure communities and ecosystemprocesses (H2

C for community traits; H2 for single ecosystem trait). Because soil microorganismsmediate many ecosystem processes, including litter decomposition and rates of nutrient mineral-ization, the formation of these communities may feed back to affect plant fitness. Solid lines indi-cate known interactions; dashed lines indicate possible interactions. Quantitative genetic patternssuch as these argue that genomic approaches will enhance our understanding of how interactingcommunity members influence ecosystem processes. Figure from Whitham and coworkers (2008).

numerous studies in diverse systems have shown that different genotypes sup-port different community members and ecosystem processes (see references inthe introduction), only a few studies have quantified the heritability of com-munity and ecosystem phenotypes (e.g., arthropod diversity on evening prim-rose – Johnson & Agrawal 2005; Johnson et al. 2006; arthropod communitycomposition, soil microbial community composition, and trophic interactionson narrowleaf cottonwood – Bailey et al. 2006; Shuster et al. 2006; Schweitzer etal. 2008; respectively). For example, Fig. 3–2 shows that the canopy arthropodcommunity on narrowleaf cottonwood (Populus angustifolia) was under stronggenetic control such that, regardless of where replicate clones of the same treegenotype were planted within a common garden, they tended to accumulate andsupport the same community of arthropods (Shuster et al. 2006). Because Shusterand coworkers used replicate clones of individual tree genotypes, they calculated



broad-sense community heritability (H2c), which estimates that genetic factors

account for approximately 60% of the variation in the canopy arthropod com-munity (H2

c = 0.60).In another common garden study of the soil microbial community, Schweitzer

et al. (2008) assessed the microbial community composition in bulk soil beneathtree canopies by using phospholipid fatty acid (PLFA) biomarkers (Fig. 3–2). PLFAsare unique to major taxonomic groups (e.g., Gram-positive and -negative bacte-ria, and fungi), and thirty different groups were identified. Their analysis founda strong tree genetic component to microbial community composition (H2

c =0.70). Schweitzer et al. (2008) also found that soil microbial biomass nitrogenexhibited high broad-sense heritability (H2 = 0.61), indicating a genetic basisfor soil nitrogen pools stored in microorganisms. This latter finding is importantbecause soil microorganisms mediate many ecosystem processes, including lit-ter decomposition, rates of nutrient mineralization, and nutrient pools. Becausethese nutrient pools are genotype dependent, the formation of different micro-bial communities beneath different tree genotypes may feed back to affect plantfitness. If so, such feedbacks would establish a crucial link between the microbialcommunity and plant fitness that could pave the way for ecosystem science to beplaced within an evolutionary framework (Bever et al. 1997; Hooper et al. 2000;Whitham et al. 2003; Bartelt-Ryser et al. 2005).

The potential for similar feedbacks on plant performance also exists above-ground in the interactions of insect herbivores and their avian predators (Fig.3–2). For example, the presence or absence of the leaf-galling aphid (Pemphigusbetae) is determined by susceptible or resistant tree genotypes. This interactionpredictably affects other trophic levels and alters the composition of a diversecommunity of fungi, insects, spiders, and avian predators (Dickson & Whitham1996; Bailey et al. 2006). In combination, these and other studies described previ-ously suggest that indirect genetic interactions among relatively few foundationspecies (e.g., tree, herbivore, predator, mutualist, and/or pathogen) and theirenvironment may structure the composition and abundance of a much largercommunity of organisms, which could then feed back to affect the performanceof individual tree genotypes.

An important goal for understanding the ecology, evolution, conservation, andmanagement of any ecosystem is to define how many foundation species (plants,animals, microbes) define a given ecosystem and their extended effects on associ-ated species. Understanding the genetics (genotypic or genetic variation therein)of foundation species in a community context is likely to be more informativethan the genetics of most other species (e.g., rare species) and should result infewer management errors than would single-factor or -population approaches.So far, our findings suggest that the study of relatively few foundation speciesin a community context can tell us much about a larger system involving manyspecies. If correct, then the conservation and management of whole ecosystemsmay be more tractable than previously thought as all species are not equallyimportant in “driving” the system. Focusing on foundation species does notimply that other organisms such as rare species are not important or deservingof preservation. It simply argues that the interactions of relatively few speciesstructure an ecosystem and that many species respond to rather than create



the conditions required by other species for their survival. If concentrating onthe community genetics of foundation species proves generally correct, it wouldgreatly simplify the dilemma of having to understand the complex interactionsof all species to make appropriate management decisions, which is a daunting ifnot impossible task.

CONSERVATION CONSEQUENCES OF HERITABLE PHENOTYPES

If different genotypes of a foundation tree species support different communitymembers and ecosystem processes as the previously mentioned heritability stud-ies demonstrate, several key predictions can be made, which are of conservationand management value.

First, if different tree genotypes support different communities, we wouldexpect that the genotypes that are genetically most similar will support themost similar communities. At both local and regional levels, Bangert and col-leagues (2006a,b) found that genetically similar cottonwoods supported similararthropod communities, whereas genetically dissimilar plants supported moredifferent communities (i.e., a genetic similarity rule hypothesis). For example, byusing a Mantel test to compare the molecular marker and arthropod communitymatrices of individual trees, we found that trees that were the most geneticallysimilar were also the most similar in their arthropod communities (Fig. 3–3).This pattern holds for trees growing in a common garden, for trees growing inthe wild in a single river (Fig. 3–3; Bangert et al. 2006a), and for trees growingthroughout the American West in multiple river systems covering 720,000 km2

(Bangert et al. 2006b). Studies with the forest tree (Eucalyptus globulus) in Aus-tralia showed a similar pattern in which the most genetically similar trees andgeographic races also supported more similar canopy communities (Barbour etal. 2009). In both studies the correlation in divergence in molecular and commu-nity variation was mediated through correlated divergence in quantitative traitssuch as leaf morphology and chemistry. Although it is well known that manyspecialist insects may show corresponding divergence that is correlated with thedivergence of their host plant species (e.g., Abbot & Withgott 2004), it appearsthat the same pattern holds for less specialized community members. From aconservation perspective, the findings of Figs. 3–2 and 3–3 argue that geneticdiversity in a foundation tree species matters for the dependent community ofmicrobes, arthropods, and vertebrates.

Second, if different tree genotypes support different communities, then greatergenetic diversity in a foundation species should be directly correlated with greatercommunity diversity. Based on this prediction, Wimp and colleagues (2004) usedamplified fragment length polymorphism (AFLP) molecular markers to quan-tify genetic diversity in eleven different stands of cottonwoods growing in ahybrid zone along the Weber River in Utah. The arthropod community was thenrecorded for the same trees, and the researchers found that stand genetic diversityaccounted for approximately 60% of the variation in the diversity of an arthropodcommunity composed of 207 species (Fig. 3–4). Similar findings were obtainedwith oaks (Quercus spp.; Tovar-Sanchez & Oyama 2006). Experimental studies



Figure 3–3: Because genetically similar trees support similar communities of organisms, (i.e.,the Genetic Similarity Rule), genetic diversity in a foundation plant species is likely to supportgreater biodiversity in the associated community. On average, Mantel tests show that arthropodcommunities become less similar as plant genetic distance increases (i.e., small genetic distanceindicates more closely related trees). Genetic distances of the common garden trees (solid circles)were based on restriction fragment length polymorphism (RFLP) markers. The genetic distancesof the naturally growing trees in the wild (open triangles) were based on AFLP marker data andinclude only the F1 and backcross hybrids, thus removing the leverage of the two pure parentalspecies from the analysis. Figure from Bangert and colleagues (2006a).

that manipulated genetic diversity with evening primrose (Oenothera biennis) andgoldenrod (Solidago altissima) also showed that genetically diverse patches sup-ported significantly greater species richness than did monocultures (Crutsingeret al. 2006; Johnson et al. 2006; respectively).

Third, if individual plant genotypes support different communities, they alsomay drive genetic differentiation and speciation in dependent community mem-bers. Several studies have found that populations of herbivores are adapted toindividual host genotypes (Karban 1989; Mopper et al. 1995, 2000; Mopper 1996;Evans et al. 2008). Because speciation may follow from locally adapted, differ-entiated populations of arthropods (Via 2001; Dres & Mallet 2002), conservinggenotypic diversity in foundation species can conserve locally adapted popu-lations of arthropods. Conserving genotypic diversity in foundation species toconserve locally adapted populations of dependent species may extend to mul-tiple trophic levels. For example, multiple herbivores (Stireman et al. 2005) andtheir parasitoids (Stireman et al. 2006) are genetically differentiated on two closelyrelated sympatric species of Solidago indicating that host plants can affect species’evolution at multiple tropic levels. A major conclusion from such studies is thatgenetic diversity is far more than just an endangered species issue; it is also impor-tant for common foundation species in which different plant genotypes supportdifferent community members.



Average cottonwood gene diversity (He)

0.14 0.16 0.18 0.20 0.22 0.24 0.26 0.28 0.30 0.32 0.34

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Figure 3–4: At the stand level, genetic diversity in a foundation tree species is highly corre-lated with the diversity of an arthropod community of 207 species. Cottonwood genetic diversitypredicted arthropod diversity at a stand level. Each point in the scatterplot represents the Shannon–Weaver index of arthropod diversity (H¢) as a function of cottonwood gene diversity (He) in thesame stand; a total of eleven stands were analyzed. The diagonal line represents the line of bestfit that describes the relationship between increasing arthropod diversity as a result of increasingcottonwood genetic diversity. Figure from Wimp and colleagues (2004).

Fourth, when different genotypes of a foundation species support differentcommunities, management practices based on species-area relationships mayneed to shift to genetic diversity-area relationships. In other words, is the species-area curve really driven by area, is it driven by the genetic diversity of the founda-tion species, or is it driven by both? To answer this question, Bangert et al. (2008)quantified the arthropod species accumulation curve for broadleaf cottonwoods(Fig. 3–5A). This curve shows that, as the arthropod communities of more trees aresampled (i.e., area), arthropod species richness increases predictably and beginsto plateau. This pattern is common and is a primary justification for the con-servation practice of preserving large areas to capture the species pool. Whenmolecular marker diversity for the same trees was analyzed to produce a molec-ular marker richness accumulation curve, the same pattern emerged. This curveshows that as the molecular markers of more trees are sampled (i.e., area), markerrichness also increases predictably and begins to plateau. The two curves areremarkably similar. Furthermore, arthropod species richness is highly correlatedwith molecular marker richness (r 2 = 0.92; Fig. 3–5B). This strong correlationraises an issue: Is the species-area curve driving biodiversity, is it the geneticdiversity of the foundation species that drives biodiversity, or is there some com-bination of the two? Although area and genetic diversity of foundation speciesare undoubtedly autocorrelated, from a manager’s perspective it is important toknow whether a landscape should be managed from an area perspective or from



80 20 R2 = 0.9234p < 0.0001

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Figure 3–5: The species-area curve is also a species-genetic diversity curve, which may affectmanagement decisions to preserve communities based on area, genetic diversity of foundationspecies, or both. (A) Scaling in which both arthropods and molecular markers scale similarly as afunction of the number of broadleaf cottonwoods sampled (sample size or number is also a proxyfor area). At their asymptotes, adequate sampling captures most of the arthropod community andgenetic diversity, respectively. (B) Consistent with the above similarity in scaling, there is a strongpositive relationship between arthropod species richness and marker richness. Because trees wereselected at random, no geographic structure is reflected in these patterns. Figure from Bangert andcolleagues (2008).

the genetic diversity of a foundation species’ perspective. Furthermore, if futureconservation efforts try to establish living repositories for individual species, it isimportant to define the genetic diversity of these repositories that will be requiredto support their dependent communities.

A COMMUNITY GENETICS PERSPECTIVE ON MINIMUMVIABLE POPULATIONS

Historically, an important concept in conservation biology is the minimum viablepopulation (MVP), which is the size of a population that, with a given probability,will ensure the existence of the population for a stated period of time (Shaffer1981; Gilpin 1987). This concept is especially important for rare and endangeredspecies whose populations are often small, highly inbred, and lacking in geneticdiversity. Although this concept attempts to understand what population sizes arerequired to save a single species, it falls short of understanding what is necessaryto save dependent community members and especially species that require asingle host species or a subset of the host’s genotypes for their survival.

An example of how the distribution, population growth rate, and evolutionof one species can be dependent on genotypic differences of another species isthat of the gall-forming mite (Aceria parapopuli) on cottonwoods. McIntyre andWhitham (2003) found that 99% of the mite’s population was concentrated onnaturally occurring F1 hybrids between narrowleaf and Fremont cottonwood (P.angustifolia, P. fremontii, respectively). Because suitable F1 hybrid hosts are rare inthe wild, the “actual” host population for these mites is a small subset of the larger



cottonwood population. Furthermore, Evans et al. (2008) showed that the mitesare even further differentiated such that the mites on the hybrids and parentalhosts are different cryptic species. Transfer experiments showed that, even amongF1 hybrids, the mites can be adapted to individual tree genotypes. Thus, eventhough cottonwoods are common trees in riparian forests, a dependent speciescan still be limited by the number of suitable host genotypes.

Even generalist species can be genetically differentiated and highly specializedat the local level (Thompson 1994). The eastern tiger swallowtail (Papilio glaucus)has a large list of host species, but at a local scale, it can be host specific (Scriber1986). Other examples are provided by Feder and colleagues (1988), Wood andKeese (1990), Roinen and coworkers (1993), and Thompson (1994). Microor-ganisms can exhibit even greater specificity. Gene-specific interactions betweenRhizobium leguminosarum bv. viciae and native Afghani pea plants (Pisum sativum)regulate symbiosis. The loss of a single gene will disrupt the symbiotic interac-tion and prevent nitrogen fixation (Vijn et al. 1993). Specificity in gene-for-geneinteractions in molecular control points between plants and microorganisms inthe rhizosphere is thought to be widespread in many foundation species (Hirschet al. 2003; Phillips et al. 2003).

Such specificity suggests that MVP sizes (Shaffer 1981) in one species may be toosmall to support important interactions with other species (see Thompson 1994as well as Chapter 10 by Waples and colleagues). Other researchers have recog-nized the weaknesses associated with the conservation of individual species ratherthan communities or ecosystems (e.g., Rohlf 1991; Simberloff 1998; Lindenmayeret al. 2007). A community genetics approach enhances our understanding of whythe genetics of foundation species are so important, provides genetically basedmechanisms to support these criticisms, and has the potential to merge differentpoints of view as it spans genes to ecosystems.

Because of these issues, Whitham and colleagues (2003) proposed the mini-mum viable interacting population (MVIP) size that represents the size of a pop-ulation needed to maintain genetic diversity at levels required by other dependentand interacting species in a community context. For example, MVP sizes for con-serving a foundation tree species are probably much smaller than the populationsize required to conserve other dependent community members that require asubset of the tree’s genotypes for their survival (MVIP). Thus, MVP representsthe lower end of the population size that is required to conserve the foundationspecies, and MVIP represents the upper end of the population size of the foun-dation species that is required to conserve the dependent community and theirinteractions. Fig. 3–6 provides an initial guide as to where the differences betweenMVP for a foundation species and MVIP for a foundation species and its depen-dent community would be expected to be highest and lowest. High communityand ecosystem heritability (H2

c) suggests that many community members andthe ecosystem processes they drive are dependent on the individual genotypesof a foundation species, whereas a low or nonsignificant H2

c suggests that thedistributions of most community members are not genotype dependent. Thus,as community heritability increases for any given foundation species, we wouldexpect that the difference between MVP and MVIP would also increase.



Community Heritability H2C

Low High

Populationsize neededto conservedependentcommunity

MVIP – Minimum Viable Interacting Population

Figure 3–6: Illustration of the hypothesized relationship between high community heritability(i.e., different genotypes of a foundation species support different communities of organisms andecosystem processes) and the population size needed to preserve the dependent community.As community heritability increases, the population size of the foundation species must increaseto support its dependent community and the ecosystem processes they promote. The minimumviable interacting population (MVIP), takes into account the genetics-based interactions amongspecies in a community context. See text for contrast of MVP and MVIP.

MVP and MVIP represent end points on the population-to-community con-tinuum. They provide a conceptual mechanism to explain why conservationefforts may flounder if they do not consider the consequences of genetic varia-tion in foundation species on the dependent community (see Chapter 9 by Lebergand colleagues). Numerous studies show that temperate and boreal trees exhibitmoderate to strong clines in ecologically important traits suggesting that pop-ulations are genetically differentiated and locally adapted (Aitken et al. 2008).Associated with this genetic structuring, common garden studies by Barbouret al. (2009) showed that different geographic races of the same eucalypt speciessupported different communities. Although current conservation strategies tar-get rare species, it may be even more important to conserve the genetic variationin foundation species with broad distributions, because individual genotypes andraces have different community and ecosystem phenotypes.

COMMUNITY PHENOTYPES OF GENETICALLY ENGINEERED ORGANISMS

Although the incorporation of novel genes into an organism through recombi-nant deoxyribonucleic acid (DNA) technology has enormous potential benefits,including increasing crop yields and reducing reliance on chemical pesticides(Avise 2003), the genes introduced into genetically engineered organisms (GEOs)may have unintended community and ecosystem phenotypes that are impor-tant to evaluate. Several issues need to be considered. First, GEOs now have beenintroduced over large areas in both industrialized and developing economies.



For example, the global area planted with transgenic crops exceeded 110 millionhectares in 2007, a 12% increase over the previous year (Lawrence 2008). Becausemany of these crops are grown as monocultures with little genetic variation, theyare, in effect, both a foundation species and a foundation genotype.

Second, there is increasing evidence that transgenic organisms can movebeyond their intended destinations where they have the potential to persist andto hybridize with native species (see Chapter 2 by Schaal and colleagues). Maximalgene-flow distances of 21 km were observed in herbicide (glyphosate)-resistantcreeping bent grass (Agrostis stolonifera L.), a wind-pollinated, out-crossing, peren-nial turf grass planted in test fields in Oregon (Watrud et al. 2004). Three yearsafter the test fields were taken out of production, 62% of plants tested wereglyphosate resistant (Zapiola et al. 2008). There is evidence that transgenic canola(Brassica napus) and sunflower (Helianthus annuus) hybridize with wild relatives,although the fitness of these hybrids is highly variable and frequently not greaterthan wild genotypes (reviewed in Chapman & Burke 2006). Recent research alsosuggests that the risk of environmental impact from horizontal gene transfer ofbacterial genes from crops to surrounding soil microorganisms is much higherthan initially supposed (Heinemann & Traavik 2004). In their review, Marvier andVan Acker (2005) concluded that movement of transgenes beyond their intendeddestinations is a “virtual certainty.”

A third reason that transgenics may have unintended ecological consequencesfor communities and ecosystems is that transgenes are designed to have sig-nificant fitness consequences (e.g., reducing herbivory, disease, or competition)thereby increasing the likelihood that transgenics will interact significantly withmembers of the communities in which they are introduced. Furthermore, cropswith stacked traits (two or more transgenes) are now more widely planted thanthose containing only insect-resistance traits (Lawrence 2008).

Transgenic plants have been shown to have nontarget community and ecosys-tem phenotypes. For example, Bt corn byproducts can enter headwater streamswhere they are stored, consumed, and transported downstream to other bodiesof water. Feeding trials in the laboratory indicate that Bt corn residues negativelyaffect nontarget stream insects (Rosi-Marshall et al. 2007). Recent meta-analyses,however, highlight the need for comparison of the effects of transgenes to thoseof traditional agricultural practices. An analysis of forty-two experiments showedthat Bt cotton and corn altered the abundance of some taxa of nontarget arthro-pods, but the effects of the transgenes were much smaller than those of traditionalpesticides (Marvier et al. 2007). Likewise, consistent effects of Bt corn, cotton,and potatoes on particular functional guilds of nontarget arthropods were notobserved (Wolfenbarger et al. 2008). A recent review of Bt plant effects on the soilbiota also found few significant impacts (Icoz & Stotzky 2008). Note that moststudies of nontarget effects of transgenic organisms are relatively short-term andthus may ignore effects that accumulate slowly or are triggered by a change inenvironmental conditions.

A community genetics analysis provides a method for quantifying the commu-nity and ecosystem phenotypes of transgenes and their heritability. Importantly,in many ecological studies, the direct effects of a trait on an organism’s phenotype(e.g., increased resistance to pest attack) may be less important than the indirect



effects on the community phenotype (e.g., increased resistance to pest attackalters competitive interactions with other species to alter community structure).The movement of transgenes into wild populations, via hybridization and intro-gression, could alter interspecific interactions, potentially resulting in changesin the distribution of the wild population and its dependent community. Fewstudies of GEOs examine the consequences of transgenes on interactions, partic-ularly indirect interactions, among organisms. In addition, subtle, initial changesin interactions between transgenic and wild populations may not be detected inshort-term studies that are frequently limited in spatial scale as well. The com-munity and ecosystem consequences of transgenes are also important to definebecause of the growing view that transgenes will escape from their intended des-tination and that they cannot be retracted after they have escaped (Marvier &Van Acker 2005). When released, some transgenes may have irreversible con-servation implications for communities and ecosystems. These possible negativeconsequences of GEOs should be considered along with their potential benefits,such as promoting agricultural efficiency and reducing pesticide use.

COMMUNITY GENETICS AND CLIMATE CHANGE

Climate change is a “wild card” in conservation and restoration. Because of con-cerns about restoring only with locally adapted genotypes, the policies of mostagencies require the use of local stock in restoration. Whereas this is a valid viewin an unchanging world, in a dynamic world facing major vegetation shifts inresponse to climate change, the “local” environment may well shift so fast or somuch that local genotypes will no longer be locally adapted (see also Aitken et al.2008). In the American Southwest, the effects of climate change are pronouncedand affect the distributions of pinyon pine (Pinus edulis), cottonwood (Populusfremontii), ponderosa pine (Pinus ponderosa), quaking aspen (Populus tremuloides),and pointleaf manzanita (Arctostaphylos pungens), which are foundation speciesof their respective communities from low elevation deserts to mountain forests(Breshears et al. 2005; Mueller et al. 2005; Gitlin et al. 2006). For example, climate-change models of Rehfeldt and colleagues (2006) predict that, by 2090, the cli-mate envelopes for both pinyon pine (P. edulis) and saguaro cactus (Carnegieagigantea) will shift out of Arizona, where they are currently foundation speciesthat define their respective communities (Fig. 3–7). Such dramatic shifts in thedistributions of these species are likely to represent both ecological and evolu-tionary events and major conservation challenges. If these shifts come about,Saguaro National Monument will no longer contain saguaros, and for saguarosto physically reach their new climate envelope in eastern Nevada, human-assistedmigration will likely be required (McLachlan et al. 2007; Aitken et al. 2008).

One factor that can potentially alleviate such dramatic shifts in distribution isthe potential for selection to favor more drought-adapted genotypes that allowspecies to persist in areas where they might otherwise go locally extinct. Forexample, Franks and colleagues (2007) found rapid evolution in flowering timeof field mustard (Brassica rapa) in response to altered growing seasons over justseven years. Postdrought descendants of this annual bloomed earlier than did



Current

Pinus edulis

Carnegiea gigantea

2060 20902030

Figure 3–7: Climate change is predicted to have rapid and major affects on the distribution offoundation plant species across the American West. Modeled climate profiles for saguaro andpinyon pine are shown for the contemporary climate and for the decades beginning in 2030,2060, and 2090 (left to right). Figure from Rehfeldt and colleagues (2006).

predrought ancestors, advancing first flowering by as much as nine days. Theintermediate flowering time of Ancestor × Descendant hybrids supports an addi-tive genetic basis for this divergence. Even vertebrate species appear capable ofrapid evolutionary responses to climate change. Over a thirty-year period, Grantand Grant (2002) observed rapid evolution in the shape and size of beaks offinches in association with climate change–driven changes in seed availability.

So, what is the community genetics connection to climate change? If cli-mate change acts as an agent of selection to alter the frequency distributionof genotypes of foundation species, then their dependent communities will alsobe affected. For example, Whitham and coworkers (2003) showed that approxi-mately 1,000 species of organisms from microbes to vertebrates were differentiallyassociated with insect-resistant and -susceptible pinyon pine (P. edulis). Recentstudies by Sthultz and colleagues (2009) showed that insect-resistant trees were3 times more likely to die than susceptible trees were during a record drought andthat the change in the distribution of resistant and susceptible phenotypes on thelandscape had changed from resistance-dominated stands to near parity. Thus,even if a foundation species survives in a given habitat, the change in its geneticstructure is likely to affect dependent community members whose distributionsare also dependent on the genotypes of the foundation plant species (see earliersections on heritable phenotypes and minimum viable populations).

Rehfeldt and colleagues (2006) used climate envelopes to predict the futuredistributions of many tree species of the western United States, including P. edulis.They concluded that P. edulis would be extirpated from Arizona within eighty



years. This prediction, however, did not include potentially drought-adaptedgenotypes of P. edulis or reflect the genetic variation among populations thatmight exist over its large geographic distribution. In contrast, a few other modelshave incorporated intraspecific genetic variation and demonstrated its potentialinfluence on climate-change projections. For example, based on provenance trialsinvolving 140 populations tested at 62 sites throughout most of the range oflodgepole pine (P. contorta), O’Neill and coworkers (2008) included into theirmodels genetic differences in the performance of these populations. Becausepopulations tend to be locally adapted, these models predicted that differentpopulations would vary greatly in their responses to climate change and thatmany populations would be maladapted to their new local environment. Thisprovenance trial approach also provides an experimental method for identifyingwhich populations or genotypes might best survive predicted climate changes.Thus, for species for which such provenance trials already exist, the use of thispowerful experimental approach could greatly enhance the precision of climate-change models.

From these examples, it would appear that climate change creates a conundrumfor conservation biologists and managers. If our management policies requirerestoration with local genotypes, in a climate-change scenario are we then plant-ing the very genotypes that are doomed to fail? Few studies with foundationspecies are in place to provide clear information for managers to make appro-priate decisions (but see O’Neill et al. 2008). We need a national network ofcommon gardens for foundation species in which genotypes from the wholerange of a species’ distribution are planted reciprocally within their current rangeand their predicted new ranges. Only with such empirical information can weidentify the specific genotypes and source populations that are best suited tocurrent and predicted future local conditions.

MANAGEMENT CONCLUSIONS

A community and ecosystem genetics approach is based on the fundamentalfinding that individual genotypes or populations of foundation species have her-itable community and ecosystem phenotypes (Fig. 3–2). Because this finding hasemerged from diverse systems on different continents, our review explores fivemanagement implications: 1) Management practices should be based on conserv-ing genetic diversity in foundation species. Because different genotypes supportdifferent communities (Figs. 3–2 and 3–3), greater biodiversity will be achieved bypreserving the greatest genetic diversity in the foundation species (e.g., Fig. 3–4).2) It is important for managers to determine if they should be managing for area,the genetic diversity of the foundation species, or some combination of both.This is due to the fact that the species-area curve (i.e., the current basis of themanagement practice of setting aside large geographical areas to capture the max-imum number of species in preserves) is also highly correlated with the geneticdiversity of foundation species-area curve (Fig. 3–5). 3) Management practices forconserving biodiversity should be based upon the minimum viable interactingpopulation (MVIP), which is likely to be much larger than the minimum viablepopulation (MVP). Because the distribution of many species can be dependent



on the genotypes of foundation species, the population size of the foundationspecies required to support all of its dependent community members is muchlarger than that needed to save the foundation species itself (Fig. 3–6). 4) Weneed management protocols that specifically quantify the unintended ecosystemeffects of genetically engineered organisms (i.e., their community and ecosystemphenotypes) as part of the evaluation process for commercial release. 5) Manag-ing for climate change by establishing provenance trials of foundation speciesthroughout their current and predicted range is needed to identify the genotypesand source populations that are most likely to survive, reproduce, and supporttheir dependent communities in a new climate. These are a few of the man-agement issues that arise when we apply a community and ecosystem geneticsapproach rather than just a population genetics approach.

As an initial step to achieve these goals, it would be especially helpful andcost effective if managers tagged and mapped the donors used for propagation(both for seeds and cuttings) and then tagged the individuals used in restora-tion plantings. Although such “bookkeeping” would represent a small fractionof the overall cost of a restoration project, the value added could be great andresult in cost savings in future restoration projects. If multiple source popula-tions and genotypes were used, managers could identify which genotypes andsource populations were best adapted to a specific planting site. Long-term data isespecially important as those genotypes that perform best under current climaticconditions may not be the best with future climatic conditions (e.g., Sthultzet al. 2009). Performance data combined with climate change models could beused to identify which source populations and genotypes might best suit a pre-dicted future climate. Because many plants used in restoration are long-lived,after tagged restoration sites are established, they can also be used for the life ofthe site to quantify the diverse communities of organisms they support as a func-tion of the individual genotypes and source populations used in the restorationproject. Because species evolve in a community context, then we must ultimatelyconserve and manage species in a community context.

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