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

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.

Can interspecies affairs in the dark lead to evolutionary innovation?

“…While transmission mode, genome size, and host dependence are well‐studied topics in molecular ecology, the effects of host hybridization on the evolution of microbial symbioses have not received much attention. Breusing et al () took a step towards a better understanding of these complex interactions and asked whether host hybridization in vesicomyid clams can lead to interspecies exchange of otherwise strictly vertically inherited bacterial symbionts. Vesicomyid clams are found at hydrothermal vents and hydrocarbon seeps across oceans (Figure c).…”

“…For example, individuals of the host mitochondrial haplotype specific for Archivesica gigas harboured the bacterial symbionts usually associated with Phreagena soyoae at Pedro's Whalefall in the eastern Pacific Ocean (Johnson, Krylova, Audzijonyte, Sahling, & Vrijenhoek, ). Besides occasional exchange with free‐living relatives or physical trade of the symbionts among sympatric eggs, Breusing et al () hypothesize host hybridization between A. gigas and P. soyoae as a new mechanism for symbiont exchange among different host species.…”

“…Images (a2), (a3), and (a4) were kindly provided by Dr. Perrine Cruaud (ORCID: 0000‐0001‐8628‐3600) at the Laboratory of Microbiology of the Extreme Environments (LMEE), Ifremer, Brest, France. (b) Breusing et al () constructed haplotype networks for host genes (mitochondrial: mtCOI; nuclear: ANT, H3), as well as symbiont genes (16S rRNA gene: sym16S) of two host species (light green = P. soyoae , dark green = Archivesica gigas ). Each circle represents a haplotype with circle size showing its frequency in the dataset.…”

“…Mixed haplotypes are shown as pie charts of light and dark green. (c1, c2) Deep sea hydrocarbon seep collection site at Pescadero Basin in the Gulf of California, Mexico from the expedition in 2015 when samples of Breusing et al () were collected in their natural habitat. An image‐use agreement was provided by the Monterey Bay Aquarium Research Institute (MBARI)…”

“…To test whether hybridization had occurred between A. gigas and P. soyoae and could possibly account for a symbiont switch, Breusing et al () developed a host genome‐wide SNP (single nucleotide polymorphism) panel for the two host species. Then, they genotyped several populations, with special focus on the population at Pedro's Whalefall, where there were elevated levels of host‐symbiont mismatches.…”