A broadscale analysis of host-symbiont cophylogeny reveals the drivers of phylogenetic congruence.

Alexander Hayward,Robert Poulin,Shinichi Nakagawa,Helene Morlon

doi:10.1111/ele.13757

Alexander Hayward, Robert Poulin + Show 2 more

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https://doi.org/10.1111/ele.13757

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Abstract

Symbioses exert substantial biological influence, with great evolutionary and ecological relevance for disease, major evolutionary transitions, and the structure and function of ecological communities. Yet, much remains unknown about the patterns and processes that characterise symbioses. A major unanswered question is the extent to which symbiont phylogenies mirror those of their hosts and if patterns differ for parasites and mutualists. Addressing this question offers fundamental insights into evolutionary processes, such as whether symbionts typically codiverge with their hosts or if diversity is generated via host switches. Here, we perform a meta-analysis of host-symbiont phylogenetic congruence, encompassing 212 host-symbiont cophylogenetic studies that include ~10,000 species. Our analysis supersedes previous qualitative assessments by utilising a quantitative framework. We show that symbiont phylogeny broadly reflects host phylogeny across biodiversity and life-history, demonstrating a general pattern of phylogenetic congruence in host-symbiont interactions. We reveal two key aspects of symbiont life-history that promote closer ties between hosts and symbionts: vertical transmission and mutualism. Mode of symbiosis and mode of transmission are intimately interlinked, but vertical transmission is the dominant factor. Given the pervasiveness of symbioses, these findings provide important insights into the processes responsible for generating and maintaining the Earth's rich biodiversity.

Highlights

Symbioses are prolonged and intimate associations between organisms of different species (Wilkinson, 2001), typically defined in terms of an interaction between a larger host organism and a smaller symbiont (Estrela et al, 2016)
Horizontal transmission should facilitate exposure to novel hosts, potentially leading to host-switching, and decreased host-symbiont phylogenetic congruence. In line with this prediction, we found that mode of transmission was a significant predictor of host-symbiont phylogenetic congruence, with the strongest effect observed for vertical transmission, followed by the effect observed for mixed modes of transmission, and with horizontal transmission showing the lowest effect size (r[vertical] = 0.636, CI = [0.561: 0C.7I0=1][;0r.3[b6o1t:h]0=.4704.5],2a1n, dCRI =2 =[00.4.13827:;0F.6ig0u0r];er4[hBoraiznodntAal]p=pe0n.4d1i9x, S3, Table S3.7)
We identified an effect of mode of transmission on host-symbiont phylogenetic congruence, finding that vertical transmission is correlated with greater congruence

Summary

Introduction

Symbioses are prolonged and intimate associations between organisms of different species (Wilkinson, 2001), typically defined in terms of an interaction between a larger host organism and a smaller symbiont (Estrela et al, 2016). Given an ancestral host-symbiont association, multiple rounds of strict codivergence will result in a symbiont phylogeny that. A BROADSCALE ANALYSIS OF HOST-SYMBIONT COPHYLOGENY REVEALS THE DRIVERS OF PHYLOGENETIC CONGRUENCE b c d e f g h. Perfect congruence is considered to be rare, due to the effects of disruptive events such as host switching (Figure 2B), extinction (Figure 2C), independent divergence (Figure 2D), or failure to diverge (Figure 2E), which all lead to incongruence in host-symbiont phylogenies (Paterson et al, 2003) (Figure 2F). Imperfect congruence can arise through host-switch divergence, referred to as host-shift speciation or pseudocospeciation (De Vienne et al, 2007; de Vienne et al, 2013), whereby repeated host switches followed by divergence events mirror host phylogeny

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