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UC Riverside UC Riverside Previously Published Works Title Fitness variation among host species and the paradox of ineffective rhizobia. Permalink https://escholarship.org/uc/item/0px6z7b1 Journal Journal of evolutionary biology, 31(4) ISSN 1010-061X Authors Pahua, VJ Stokes, PJN Hollowell, AC et al. Publication Date 2018-04-01 DOI 10.1111/jeb.13249 Peer reviewed eScholarship.org Powered by the California Digital Library University of California doi: 10.1111/jeb.13249 Fitness variation among host species and the paradox of ineffective rhizobia V. J. PAHUA*, P. J. N. STOKES†,A.C.HOLLOWELL*,J.U.REGUS*, K. A. GANO-COHEN*, C. E. WENDLANDT†,K.W.QUIDES*,J.Y.LYU*& J. L. SACHS*†‡ *Department of Evolution Ecology and Organismal Biology, University of California, Riverside, CA, USA †Department of Botany and Plant Sciences, University of California, Riverside, CA, USA ‡Institute for Integrative Genome Biology, University of California, Riverside, CA, USA Keywords: Abstract Acmispon strigosus; Legumes can preferentially select beneficial rhizobial symbionts and sanction Bradyrhizobium; ineffective strains that fail to fix nitrogen. Yet paradoxically, rhizobial popu- cheater symbionts; lations vary from highly beneficial to ineffective in natural and agricultural host control; soils. Classic models of symbiosis focus on the single dimension of symbiont ineffective symbionts; cost-benefit to sympatric hosts, but fail to explain the widespread persistence trade-offs. of ineffective rhizobia. Here, we test a novel framework predicting that spa- tio-temporal and community dynamics can maintain ineffective strains in rhizobial populations. We used clonal and multistrain inoculations and quantitative culturing to investigate the relative fitness of four focal Bradyrhizobium strains varying from effective to ineffective on Acmispon strigosus. We found that an ineffective Bradyrhizobium strain can be sanc- tioned by its native A. strigosus host across the host’s range, forming fewer and smaller nodules compared to beneficial strains. But the same ineffective Bradyrhizobium strain exhibits a nearly opposite pattern on the broadly sym- patric host Acmispon wrangelianus, forming large nodules in both clonal and multistrain inoculations. These data suggest that community-level effects could favour the persistence of ineffective rhizobia and contribute to varia- tion in symbiotic nitrogen fixation. instance, in the legume-rhizobium symbiosis, rhizobial Introduction bacteria instigate the formation of nodules on legume Environmentally acquired bacteria provide diverse roots and fix atmospheric nitrogen for their host in benefits to plant hosts, including enhanced growth, exchange for photosynthates. Rhizobial infections com- drought and stress tolerance (Sachs et al., 2010a; monly range from highly effective (i.e. enhancing Bresson et al., 2013; Antonio Lucas et al., 2014; legume growth via nitrogen fixation) to ineffective (i.e. Coleman-Derr & Tringe, 2014), and improved outcomes non-nitrogen fixing and not benefiting host growth; in interactions with competitors, herbivores and patho- Burdon et al., 1999; Sachs et al., 2010a), but the gens (Fravel, 1988; van Loon et al., 1998; Hassan et al., maintenance of this variation is poorly understood. 2010; Friesen et al., 2011; Pieterse et al., 2014). The fit- Legumes can minimize the impact of costly rhizobial ness effects of these bacterial associates often vary infections by discriminating against ineffective rhizobia widely (Burdon et al., 1999; Heath & Tiffin, 2007; during nodule formation (partner choice; Devine et al., Rodrigues et al., 2008; Sachs & Simms, 2008). For 1990; Heath & Tiffin, 2009; Sachs et al., 2010b) and by reducing within-nodule growth rates of ineffective rhi- zobia (sanctions; Kiers et al., 2003; Simms et al., 2006; Correspondence: Joel L. Sachs, Department of Evolution Ecology and Sachs et al., 2010b; Oono et al., 2011; Regus et al., Organismal Biology, University of California, Riverside, CA 92521, 2014, 2015). These host control traits are predicted to USA. lead to the extirpation of ineffective rhizobia (Denison, Tel.: +1 951 827 6357; fax: +1 951 827 4286; e-mail: [email protected] 2000; Simms & Taylor, 2002; West et al., 2002a, b; ª 2018 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY. J. EVOL. BIOL. JOURNAL OF EVOLUTIONARY BIOLOGY ª 2018 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY 1 2 V. J. PAHUA ET AL. Sachs et al., 2004; Foster & Wenseleers, 2006). Despite variation could be driven by shifting selection mosaics in the apparent efficiency of host control by legumes co-evolving host–symbiont populations, or if there is (Regus et al., 2014, 2015), ineffective rhizobia are wide- negative frequency-dependent selection upon ineffective spread in natural and agricultural populations (Quigley rhizobia (Bever, 1999; Thompson, 2005; Steidinger & et al., 1997; Moawad et al., 1998; Burdon et al., 1999; Bever, 2014, 2016). Denton et al., 2000; Chen et al., 2002; Collins et al., Here, we investigated the maintenance of ineffective 2002; Sachs et al., 2010a). The persistence of ineffective rhizobia in native Acmispon-Bradyrhizobium symbioses in rhizobia remains a paradox with profound impacts on California. Acmispon strigosus (formerly Lotus strigosus; the fitness of wild plants and the success of crops that Brouillet, 2008) has been demonstrated to favour effec- are enhanced by bacterial symbionts (Triplett & Sad- tive over ineffective Bradyrhizobium genotypes with owsky, 1992; Sachs & Simms, 2008; Yates et al., 2011; partner choice and sanctions (Sachs et al., 2010b). The Friesen, 2012; Heath & Stinchcombe, 2014; Sachs, capacity of A. strigosus to reward beneficial strains and 2015). punish ineffective strains appears robust to wide varia- Novel models of symbiosis predict key roles for spatio- tion in soil nitrogen and to growth season (Regus et al., temporal variation and host community dynamics in the 2014, 2015), suggesting that G 9 E interactions might maintenance of ineffective symbionts (Heath & Stinch- be less important in the maintenance of variation in combe, 2014; Steidinger & Bever, 2014, 2016; Bever, this system relative to other sources of fitness variation. 2015). Mutation-selection balance is a useful null model We estimated both the fitness effects (upon hosts) and for the maintenance of ineffective rhizobia, wherein fitness of four focal Bradyrhizobium strains that were ineffective mutants evolve via deleterious mutations but previously shown to range from effective to ineffective are slowly purged from populations by purifying selec- on sympatric Acmispon hosts from the Bodega Marine tion (Van Dyken et al., 2011; Smith et al., 2014). In con- Reserve in Northern California (BMR) (Sachs et al., trast, spatio-temporal selection models predict scenarios 2010a). To investigate spatially variable selection in which ineffective symbionts are maintained in popula- among host populations (i.e. G 9 G), we inoculated tions above frequencies expected by mutation, including hosts gathered from six A. strigosus populations across a (i) coexistence of effective and ineffective symbionts dri- 700-km transect of California. To investigate fitness ven by fitness variation in different host species, (ii) spa- variation among host species that could favour ineffec- tially variable selection and (iii) temporally variable tive rhizobia, the four Bradyrhizobium strains were sepa- selection (Heath & Stinchcombe, 2014). Coexistence of rately inoculated onto five sympatric Acmispon species, effective and ineffective rhizobia can be maintained if including Acmispon angustissimus, Acmispon heermannii, rhizobial fitness varies dependent on the host species, for Acmispon micranthus, A. strigosus and Acmispon wrangelia- instance if ineffective rhizobia exhibit a more diverse nus. All of these species (except for the non-native array of host species than effective genotypes, superior A. angustissimus) coexist broadly across coastal California fitness in a subset of host species or superior fitness in and are often syntopic with A. strigosus (www.calfora. the rhizospheres of some hosts (Denison & Kiers, 2004; org). On two close relatives of A. strigosus, including Sachs & Simms, 2008; Friesen & Mathias, 2010; Sachs A. heermannii and A. wrangelianus (Allan & Porter, et al., 2011). Spatially variable selection models predict 2000), we also conducted co-infections combining that the fitness of a rhizobial genotype varies over space Bradyrhizobium genotypes that were previously shown depending on the local host’s capacity to reward or sanc- to range from effective to ineffective on sympatric tion that strain (i.e. G 9 G interactions; Simonsen & A. strigosus. Finally, to examine the potential for tempo- Stinchcombe, 2014; Steidinger & Bever, 2014) or rally variable selection, we analysed previously pub- depending on spatially variable soil or environmental lished inoculation data using the four Bradyrhizobium conditions, [i.e. G 9 E interactions (Lau et al., 2012)]. strains on A. strigosus seeds from different seed source Thus, an ineffective rhizobium that has inferior fitness in years at BMR. Subsequently, we conducted a parallel its sympatric host plant population (e.g. Sachs et al., inoculation experiment using A. strigosus seeds from six 2010b; Regus et al., 2014, 2015), might achieve superior different source years from BMR and compared the fit- fitness as it invades novel host genotypes and or soils. ness and fitness effects of effective and ineffective Research has demonstrated that both rhizobial effective- Bradyrhizobium strains.