Coevolutionary diversification creates nested-modular structure in phage–bacteria interaction networks

Abstract

One contribution of 11 to a Theme Issue 'Modelling biological evolution: recent progress, current challenges and future direction'. Phage and their bacterial hosts are the most diverse and abundant biological entities in the oceans, where their interactions have a major impact on marine ecology and ecosystem function. The structure of interaction networks for natural phage-bacteria communities offers insight into their coevolutionary origin. At small phylogenetic scales, observed communities typically show a nested structure, in which both hosts and phages can be ranked by their range of resistance and infectivity, respectively. A qualitatively different multi-scale structure is seen at larger phylogenetic scales; a natural assemblage sampled from the Atlantic Ocean displays large-scale modularity and local nestedness within each module. Here, we show that such 'nested-modular' interaction networks can be produced by a simple model of host-phage coevolution in which infection depends on genetic matching. Negative frequencydependent selection causes diversification of hosts (to escape phages) and phages (to track their evolving hosts). This creates a diverse community of bacteria and phage, maintained by kill-the-winner ecological dynamics. When the resulting communities are visualized as bipartite networks of who infects whom, they show the nested-modular structure characteristic of the Atlantic sample. The statistical significance and strength of this observation varies depending on whether the interaction networks take into account the density of the interacting strains, with implications for interpretation of interaction networks constructed by different methods. Our results suggest that the apparently complex community structures associated with marine bacteria and phage may arise from relatively simple coevolutionary origins.

Modelling biological evolution: recent progress, current challenges and future direction

“…The authors progressively show where each approximation will be sufficient and where a more complex model is needed to be used to correctly describe the system, at least qualitatively. Beckett & Williams [2] elegantly demonstrate that a very simple model of bacteriaphage interaction can result in patterns which are in very good agreement with those observed in the real ocean. On the contrary, Staň ková et al [16] show that simplifying a description of a predator-prey system by neglecting the energy level of the individuals within populations can result in erroneous conclusions regarding the optimal strategy of organisms within a population.…”

“…Beckett & Williams [2] consider another mechanism of diversification and speciation as a result of coevolution in multi-species host -parasite systems. As a study case, they investigate evolution of biodiversity in a community of bacteria and phages in the ocean.…”

“…Three of the contributions within this issue focus on revealing the mechanisms of high biodiversity and species creation [1][2][3]. Yamaguchi & Iwasa [1] consider a particularly important case of speciation called allopatric speciation, which is caused by accumulating genetic divergence owing to geographical isolation of populations (e.g.…”

Revealing in-block nestedness: Detection and benchmarking

“…The existence of in-block nested structures affects the debate around population dynamics, in ecology especially, in terms of which patterns maximize survival [5] and why. Our methodological contribution thus uncovers the need for models-beyond host-parasite [49,50]-that explain how networks transition between possible configurations: from modular to combined to purely nested architectures, as suggested by the emergence of collective attention processes [9], or from nested to combined architectures, as one would expect in a growing, but highly structured, system with increasing specialization. Noteworthy, it is not clear whether these processes are reversible, as they may respond to different systemwide adaptive processes.…”

Bacteria–phage coevolution as a driver of ecological and evolutionary processes in microbial communities

“…Results of several laboratory characterizing the ecological effects of phages on their hosts are consistent with a role for phages in maintaining bacterial diversity (Harcombe & Bull, 2005; Brockhurst et al , 2006), and the introduction of narrow host range phages to replicate experimental, two species communities of marine bacteria significantly altered the biomass of the nonhost species (Middelboe et al , 2003). However, how coevolution between bacteria and phages within a complex community setting might influence the interaction network and microbial diversity remain open questions (Beckett & Williams, 2013). …”