Transmission, relatedness, and the evolution of cooperative symbionts

Abstract

Cooperative interactions between species, termed mutualisms, play a key role in shaping natural ecosystems, economically important agricultural systems, and in influencing human health. Across different mutualisms, there is significant variation in the benefit that hosts receive from their symbionts. Empirical data suggest that transmission mode can help explain this variation: vertical transmission, where symbionts infect their host's offspring, leads to symbionts that provide greater benefits to their hosts than horizontal transmission, where symbionts leave their host and infect other hosts in the population. However, two different theoretical explanations have been given for this pattern: firstly, vertical transmission aligns the fitness interests of hosts and their symbionts; secondly, vertical transmission leads to increased relatedness between symbionts sharing a host, favouring cooperation between symbionts. We used a combination of analytical models and dynamic simulations to tease these factors apart, in order to compare their separate influences and see how they interact. We found that relatedness between symbionts sharing a host, rather than transmission mode per se, was the most important factor driving symbiont cooperation. Transmission mode mattered mainly because it determined relatedness. We also found evolutionary branching throughout much of our simulation, suggesting that a combination of transmission mode and multiplicity of infections could lead to the stable coexistence of different symbiont strategies.

The Evolution of Mutualistic Dependence

“…This stabilizing mechanism is important for Prediction One because vertically transmitted microbial mutualisms have been associated with the evolution of higher dependencies. This is because vertical transmission increases relatedness between symbionts sharing a host (Leeks et al 2019), which is important for the stability of mutualisms as it promotes cooperation between symbionts (Foster & Wenseleers 2006).…”

Cooperation and Conflict Within the Microbiota and Their Effects On Animal Hosts

“…Intriguingly, the evolution of such strong dependencies is often associated with a shift from horizontal (environmental) to vertical (parent-offspring) symbiont transmission (Frank, 1996a;Fisher et al, 2017). This shift can further reinforce the positive feedback between mutual dependencies and the mutual benefits of symbiosis, because vertical transmission increases the scope for host-beneficial cooperation among symbionts by ensuring high symbiont relatedness (Leeks et al, 2019). It is noteworthy that such high levels of symbiont relatedness can also be achieved among horizontally transmitted symbionts, for instance by imposing strong host control on immigration (as in the squid-Vibrio system; Nyholm and McFall-Ngai, 2004).…”

Can Differences in Symbiont Transmission Mode Explain the Abundance and Distribution of Fungus-Growing Termites in West Africa?

“…Theory predicts that there are two main reasons why associations with uniparental, vertical symbiont transmission should have less conflict than those with horizontal transmission (Frank, 1994(Frank, , 1995(Frank, , 1996(Frank, , 1997(Frank, , 1998Foster and Wenseleers, 2006;Leeks et al, 2019), and hence may be more successful. First, uniparental, vertical transmission results in symbionts being closely related (generally clones).…”

“…Thus symbiont-host conflict is reduced. A recent modeling and simulation study implies that both, relatedness and fitness alignment, influence the level of cooperation evolving between hosts and symbionts but that relatedness is more important than fitness alignment to explain symbiont cooperation (Leeks et al, 2019).…”

“…Evolutionary theory predicts that the transmission mode of a symbiont can be an important factor in explaining the degree of cooperation and conflict in symbiotic associations, and thus their "success" (Frank, 1994(Frank, , 1996(Frank, , 1997(Frank, , 1998Foster and Wenseleers, 2006;Leeks et al, 2019). Associations in which symbiont offspring are strictly co-transmitted with host offspring to the next generation (vertical transmission) are predicted to have less conflict than associations in which the symbiont can disperse independently of their host and infect new hosts (horizontal transmission).…”