Herbivory eliminates fitness costs of mutualism exploiters

Abstract

SummaryA common empirical observation in mutualistic interactions is the persistence of variation in partner quality and, in particular, the persistence of exploitative phenotypes. For mutualisms between hosts and symbionts, most mutualism theory assumes that exploiters always impose fitness costs on their host.We exposed legume hosts to mutualistic (nitrogen-fixing) and exploitative (non-nitrogenfixing) symbiotic rhizobia in field conditions, and manipulated the presence or absence of insect herbivory to determine if the costly fitness effects of exploitative rhizobia are contextdependent.Exploitative rhizobia predictably reduced host fitness when herbivores were excluded. However, insects caused greater damage on hosts associating with mutualistic rhizobia, as a consequence of feeding preferences related to leaf nitrogen content, resulting in the elimination of fitness costs imposed on hosts by exploitative rhizobia.Our experiment shows that herbivory is potentially an important factor in influencing the evolutionary dynamic between legumes and rhizobia. Partner choice and host sanctioning are theoretically predicted to stabilize mutualisms by reducing the frequency of exploitative symbionts. We argue that herbivore pressure may actually weaken selection on choice and sanction mechanisms, thus providing one explanation of why host-based discrimination mechanisms may not be completely effective in eliminating nonbeneficial partners.

Standing genetic variation in host preference for mutualist microbial symbionts

“…When T173 was inoculated as a single strain on M. lupulina, we observed faster plant death compared with uninoculated controls and 100% mortality when plants produced their third true leaf (on average), well before flowering [31]. When supplemented with high nitrogen fertilizer, the exploiter reduced host biomass and delayed flowering compared with uninoculated controls [31]. We confirmed strain identity on agar media with differing antibiotic resistance profiles: T173 can be distinguished from RB7 by high resistance to kanamycin and neomycin on agar plates [51].…”

“…Bromfield et al [50] collected T173 from a field where M. albus and M. lupulina co-occur, and it thus represents a strain that M. lupulina can potentially encounter [51]. Previous phylogenetic analysis indicates that T173 nests within the Ensifer clade of mutualist rhizobia, including the mutualist rhizobia strain RB7 used in this study [31,51]. T173 forms non-fixing nodules on multiple legume hosts in the Medicago genus and its original host, Melilotus alba [51].…”

“…While there is debate on the origin and the maintenance of these mechanisms [20 -23], their viability as an evolutionary stable state [15][16][17]24], and how we can distinguish between them in natural systems [20,22,25], all three mechanisms share a common outcome: the host increases the relative fitness of more beneficial partners and/or decreases the relative fitness of less beneficial or exploitative partners. Given the recurrent observation of exploitative partners [4,8,26], selection on stabilizing mechanisms is predicted to be strong because exploitative symbionts are assumed to have negative effects on host fitness [13,16,[27][28][29][30] (but see [31]). If there is a cost to stabilizing mechanisms, in the absence of exploiters, selection will favour the loss of host stabilizing traits [17].…”

Using niche breadth theory to explain generalization in mutualisms

“…If partner populations are highly structured, such that partner variation is largely among mutualists rather than within an individual mutualist's local sphere of influence, individual mutualists will have little variation on which to exert selection (Akc ßay 2017). In a field experiment, the presence of herbivores determined whether legumes with effective rhizobia outperformed legumes that had also been inoculated with an "exploiter" rhizobia strain that does not fix nitrogen (Simonsen and Stinchcombe 2014); the benefit of effective rhizobia observed when herbivores were excluded vanished when herbivores were present, because insects preferentially consumed the nitrogen-rich leaves of plants with nitrogenfixing rhizobia (Fig. Moreover, variation in partner quality that is observable under other conditions might also be masked by the presence of a third party.…”

Third-party mutualists have contrasting effects on host invasion under the enemy-release and biotic-resistance hypotheses

“…However, beneficial microbes may be key players in plant invasions by impacting plant growth and reproduction, increasing plant tolerance to biotic and abiotic stress, and mediating volatile production (Pineda et al 2010;Friesen et al 2011;Turner et al 2013;Schlaeppi and Bulgarelli 2015). Microbes could be instrumental in the success of invasive plants against the background of antagonistic herbivores that would normally prevent plant establishment (Dean et al 2014;Simonsen and Stinchcombe 2014). When cucumbers were treated with plant growth-promoting bacteria, it resulted in higher growth but there was an antagonistic affect on the herbivore population (Zehnder et al 1997).…”