Human selection and the relaxation of legume defences against ineffective rhizobia

Abstract

Enforcement mechanisms are thought to be important in maintaining mutualistic cooperation between species. A clear example of an enforcement mechanism is how legumes impose sanctions on rhizobial symbionts that fail to provide sufficient fixed N 2 . However, with domestication and breeding in high-soil-N environments, humans may have altered these natural legume defences and reduced the agricultural benefits of the symbiosis. Using six genotypes of soya beans, representing 60 years of breeding, we show that, as a group, older cultivars were better able to maintain fitness than newer cultivars (seed production) when infected with a mixture of effective and ineffective rhizobial strains. Additionally, we found small differences among cultivars in the ratio of effective : ineffective rhizobia released from their nodules, an indicator of future rhizobial strain fitness. When infected by symbionts varying in quality, legume defences against poor-quality partners have apparently worsened under decades of artificial selection.

Engineering Microbiomes to Improve Plant and Animal Health

“…Lastly, we predict that host-mediated microbiome engineering will often be more efficient using wild hosts rather than hosts that have experienced domestication, or adaptation to microbially depauperate laboratory environments. This is because genes that enable hosts to control interactions with microbes may have been lost during domestication [31,43]), and agricultural soil microbiomes likely varied greatly between successive plant generations in the absence of host-microbiome co-propagation. In contrast to domesticated plants, however, both honeybees and their vertically-transmitted gut microbes may have been shaped by artificial selection during domestication, and both wild and domesticated honeybees may therefore be suitable models for microbiome engineering.…”

“…Compared to wild ancestors, therefore, domesticated plants may have lost the full capacity for host control and symbiont choice to shape their acquired microbiomes [43]. Consequently, host-mediated engineering of microbiomes may be more successful in undomesticated than in domesticated hosts when selecting on such environmentally acquired microbiomes.…”

“…First, co-dependency of microbial partners reduces the chance that one of the partners is lost from the microbiome [66,67]. Second, symbiont choice exerted by a host can differentially acquire, amplify and retain specific microbial types with beneficial effects on host fitness [36,37,[42][43][44][45][46][47][48][49][50], again reducing turnover. Microbiomes can also sometimes be inherently stable, because they quickly reassemble to an original state if disturbed (socalled 'community resilience') and because they are difficult to invade once established (socalled 'community resistance') [68].…”

“…The efficacy of microbiome engineering derives from host control, the suites of traits that animals and plants have evolved to selectively recruit beneficial microbes into symbiosis, reward beneficial genotypes, and exclude or sanction ineffective symbionts [18,36,38,[42][43][44][45][46][47][48][49]. At the initiation of a host-microbe interaction, host control occurs via partner choice or screening, in which the host selectively alters the subset of microbes that are allowed to colonize or persist in association with the host (e.g., via resistance, immunity, and genotypic specificity [50,51]).…”

Plant species differ in their ability to reduce allocation to non‐beneficial arbuscular mycorrhizal fungi

“…Kiers et al (2007) showed that newer cultivars of soybeans did not maintain high yields when inoculated with both a good and a bad rhizobial strain, while older cultivars did, possibly indicating that newer cultivars had lost the capacity to sanction. However, this finding is unlikely to explain natural variation in sanction strength.…”