Host sanctions and the legume–rhizobium mutualism

Abstract

Explaining mutualistic cooperation between species remains one of the greatest problems for evolutionary biology. Why do symbionts provide costly services to a host, indirectly benefiting competitors sharing the same individual host? Host monitoring of symbiont performance and the imposition of sanctions on 'cheats' could stabilize mutualism. Here we show that soybeans penalize rhizobia that fail to fix N(2) inside their root nodules. We prevented a normally mutualistic rhizobium strain from cooperating (fixing N(2)) by replacing air with an N(2)-free atmosphere (Ar:O(2)). A series of experiments at three spatial scales (whole plants, half root systems and individual nodules) demonstrated that forcing non-cooperation (analogous to cheating) decreased the reproductive success of rhizobia by about 50%. Non-invasive monitoring implicated decreased O(2) supply as a possible mechanism for sanctions against cheating rhizobia. More generally, such sanctions by one or both partners may be important in stabilizing a wide range of mutualistic symbioses.

Altruism in insect societies and beyond: voluntary or enforced?

“…After such punishment, cleaner fish act more cooperatively and are less likely to feed on mucus [63,64]. Similar examples occur in the mutualisms between yucca plants and their yucca moth pollinators [53,54] and between legume plants and nitrogen-fixing bacteria, in which plants sanction bacteria that fail to fix nitrogen by cutting resources to root nodules containing such bacteria [55].…”

“…Enforced cooperation in insect and vertebrate societies and interspecific mutualisms. (a) Worker policing prevents workers from reproducing in the honeybee Apis mellifera [6]; (b) queen policing (inset) prevents most workers from reproducing successfully in the bumblebee Bombus terrestris [18]; (c) a worker with active ovaries is aggressed in the queenless ant Harpegnathos saltator [19]; (d) in the honeybee, differential feeding forces most larvae to develop as workers; only larvae reared in royal cells (arrow) can develop as queens [1,7]; (e) subordinate workers from the allodapine bee Exoneura bicolor are evicted from the nest when they have been in contact with a foreign male [39]; (f) a worker that attempted to overthrow the breeder female is punished in the queenless ant Dinoponera quadriceps [40]; (g) in the cooperatively breeding cichlid Neolamprologus pulcher, subordinates that do not help look after the eggs and fry are evicted [57]; (h) rhesus monkeys (Macaca mulatta) who do not share food are punished [58]; (i) in meerkats (Suricata suricata) dominant females prevent successful breeding by subordinates [62]; (j) soybean plants (Glycine max) sanction root nodule bacteria that do not fix nitrogen, as shown by this split root experiment [55]. …”

“…Coercion and enforced cooperation are not restricted to insect societies but also occur in vertebrate [12,50] including human [51,52] societies and multispecies mutualisms [53][54][55] (Figure 1). In contrast to insect societies, however, in which coercion typically promotes inequality in a group composed of related individuals [5], in human society and in mutualisms, coercion often promotes fairness and reduces exploitation or cheating in groups with low or zero relatedness [51,54].…”

Punish or perish? Retaliation and collaboration among humans

“…Economists use experimental games to study the effects of positive and negative incentives (i.e. reward and punishment) on our propensity to collaborate [6,7]; anthropologists visit small-scale societies to measure the culture-dependence and universality of norms that enforce cooperation [8]; psychologists study the often sub-conscious cues eliciting emotions that lead to helping behaviour or moralistic aggression [9][10][11]; neurologists use magnetic resonance techniques to correlate social dilemmas with brain activities [12,13]; game theorists modify their utility functions to take account of non-monetary concerns [14,15]; biologists look for signs of policing and sanctions in bees or bacteria [16,17]; and political scientists attempt to improve governance of institutions promoting collective actions [18,19]. Trans-disciplinary dialogues are in full swing, although communication sometimes needs improving [20].…”

An experimental and modelling exploration of the host-sanction hypothesis in legume–rhizobia mutualism

“…Decreased nodular rhizobial viability and/or early nodule senescence have been proposed as plant host sanctions against non N 2 fixing, cheating rhizobia (Denison, 2000;Kiers et al, 2003Kiers et al, , 2006. A decrease in rhizobial viability was reported when N 2 -fixing rhizobia were 'forced' to cheat soybean plants by replacing normal, N 2 containing atmosphere by an Ar:O 2 mixture (Kiers et al, 2003(Kiers et al, , 2006.…”