Evolution of division of labour in mutualistic symbiosis

Abstract

<jats:p>Mutualistic symbiosis can be regarded as interspecific division of labour, which can improve the productivity of metabolites and services but deteriorate the ability to live without partners. Interestingly, even in environmentally acquired symbiosis, involved species often rely exclusively on the partners despite the lethal risk of missing partners. To examine this paradoxical evolution, we explored the coevolutionary dynamics in symbiotic species for the amount of investment in producing their essential metabolites, which symbiotic species can share. Our study has shown that, even if obtaining partners is difficult, ‘perfect division of labour’ (PDL) can be maintained evolutionarily, where each species perfectly specializes in producing one of the essential metabolites so that every member entirely depends on the others for survival, i.e. in exchange for losing the ability of living alone. Moreover, the coevolutionary dynamics shows multistability with other states including a state without any specialization. It can cause evolutionary hysteresis: once PDL has been achieved evolutionarily when obtaining partners was relatively easy, it is not reverted even if obtaining partners becomes difficult later. Our study suggests that obligate mutualism with a high degree of mutual specialization can evolve and be maintained easier than previously thought.</jats:p>

Multiple bacterial partners in symbiosis with the nudibranch mollusk Rostanga alisae

“…from a cold seep area 11 and five extracellular symbionts for the gutless oligochaete worm Olavius algarvensis 34 . However, in these cases, symbioses involving bacteria and marine invertebrates are either endosymbiotic microbes co-occurring inside the host bacteriocytes 5 , 11 or ectosymbiotic microbes associated with the external surfaces of the animals 3 , 4 , 9 , 15 , 34 , with the exception of scaly-foot snail from hydrothermal vents having partnerships simultaneously with epi- and endosymbiontic microbes 35 .…”

“…Symbiotic associations between marine invertebrates and microbes are ubiquitous and play an important role in the ecology and evolution of species 1 – 3 . In the marine environment, the symbiosis of invertebrates with photoautotrophic microalgae in the photic zone and the symbiosis with chemoautotrophic bacteria, found in extreme habitats such as deep-sea water and hydrothermal vents or cold seeps, are the most widely distributed and well-studied associations 1 , 4 .…”

The evolution of partner specificity in mutualisms

“…One crucial factor in the development of complex mutualism is partner specificity, the degree to which one organism preferentially interacts with a single partner-species (Chomicki et al, 2020), which has been examined in numerous systems in which partners are acquired horizontally from the surrounding environment including legume-Rhizobium, figwasp, and damselfish-sea anemone mutualisms (Wang et al, 2012; Bronstein, 1987). The prevalence of partner specificity within horizontally transmitted interactions is difficult to explain given that there is a fitness cost associated with a mismatch between a host and its symbiont (Uchiumi and Sasaki, 2020; Batstone et al, 2020). Because specificity plays a pivotal role in shaping the stability, niche, and coevolutionary dynamics of mutualisms (Chomicki et al, 2020; Harrison et al, 2018; Uchiumi and Sasaki, 2020), variation in partner specificity may be explained by incorporating partner cooperation into a theoretical framework to examine how specificity and cooperation co-evolve in horizontally transmitted partnerships.…”

“…The prevalence of partner specificity within horizontally transmitted interactions is difficult to explain given that there is a fitness cost associated with a mismatch between a host and its symbiont (Uchiumi and Sasaki, 2020; Batstone et al, 2020). Because specificity plays a pivotal role in shaping the stability, niche, and coevolutionary dynamics of mutualisms (Chomicki et al, 2020; Harrison et al, 2018; Uchiumi and Sasaki, 2020), variation in partner specificity may be explained by incorporating partner cooperation into a theoretical framework to examine how specificity and cooperation co-evolve in horizontally transmitted partnerships.…”

Life history and the evolutionary loss of parental care

“…Conceptually, understanding the factors that favour the evolutionary loss of care is important, as the conditions that give rise to the loss of care are not necessarily expected to be simply the opposite of those that give rise to the origin of care. Evolutionary hysteresis refers to a situation in which the evolution of a system depends on the history of that system [30], and evolutionary hysteresis can create evolutionary tipping points in which it can become more difficult, or in some cases relatively easy, to lose a trait or strategy across evolutionary time [30][31][32]. Evolutionary hysteresis has previously been found to be important in non-parental-care contexts.…”