Host hybridization as a potential mechanism of lateral symbiont transfer in deep-sea vesicomyid clams.

Corinna Breusing,Curtis R Young,Robert C Vrijenhoek,Shannon B Johnson

doi:10.1111/mec.15224

Corinna Breusing, Curtis R Young + Show 2 more

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https://doi.org/10.1111/mec.15224

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Abstract

Deep‐sea vesicomyid clams live in mutualistic symbiosis with chemosynthetic bacteria that are inherited through the maternal germ line. On evolutionary timescales, strictly vertical transmission should lead to cospeciation of host mitochondrial and symbiont lineages; nonetheless, examples of incongruent phylogenies have been reported, suggesting that symbionts are occasionally horizontally transmitted between host species. The current paradigm for vesicomyid clams holds that direct transfers cause host shifts or mixtures of symbionts. An alternative hypothesis suggests that hybridization between host species might explain symbiont transfers. Two clam species, Archivesica gigas and Phreagena soyoae, frequently co‐occur at deep‐sea hydrocarbon seeps in the eastern Pacific Ocean. Although the two species typically host gammaproteobacterial symbiont lineages marked by divergent 16S rRNA phylotypes, we identified a number of clams with the A. gigas mitotype that hosted symbionts with the P. soyoae phylotype. Demographic inference models based on genome‐wide SNP data and three Sanger sequenced gene markers provided evidence that A. gigas and P. soyoae hybridized in the past, supporting the hypothesis that hybridization might be a viable mechanism of interspecific symbiont transfer. These findings provide new perspectives on the evolution of vertically transmitted symbionts and their hosts in deep‐sea chemosynthetic environments.

Highlights

Host–microbe symbioses are universal phenomena that are considered key drivers of evolutionary innovation (Archibald, 2015; Brucker & Bordenstein, 2012; McFall‐Ngai, 2008; McFall‐Ngai et al, 2013)
Ikuta et al (2016) recently showed that the symbiont of Phreagena okutanii spends part of its life attached to the surface of the host's eggs, thereby strength‐ ening Stewart et al.'s (2008) argument that direct contact between eggs or eggs and host tissues can lead to lateral symbiont transfer between co‐occurring clam species
Using demographic inference models based on ge‐ nome‐wide SNPs as well as traditional DNA markers, we investi‐ gated the hypothesis that hybridization between the two species might be a mechanism of horizontal symbiont transfer in this sys‐ tem and examined the nature of this gene flow between the taxa

Summary

| INTRODUCTION

Host–microbe symbioses are universal phenomena that are considered key drivers of evolutionary innovation (Archibald, 2015; Brucker & Bordenstein, 2012; McFall‐Ngai, 2008; McFall‐Ngai et al, 2013). Ikuta et al (2016) recently showed that the symbiont of Phreagena okutanii (previously Calyptogena okutanii) spends part of its life attached to the surface of the host's eggs, thereby strength‐ ening Stewart et al.'s (2008) argument that direct contact between eggs or eggs and host tissues can lead to lateral symbiont transfer between co‐occurring clam species. While these studies consid‐ ered the possibility of host hybridization or environmental symbi‐ ont acquisition unlikely, these hypotheses have not been directly addressed by previous analyses. Using demographic inference models based on ge‐ nome‐wide SNPs as well as traditional DNA markers, we investi‐ gated the hypothesis that hybridization between the two species might be a mechanism of horizontal symbiont transfer in this sys‐ tem and examined the nature of this gene flow between the taxa

| MATERIAL AND METHODS

Findings

| DISCUSSION