Broad North Atlantic distribution of a meiobenthic annelid – against all odds

Katrine Worsaae,Áki Vang,Alexandra Kerbl,Brett C. Gonzalez

doi:10.1038/s41598-019-51765-x

Abstract

DNA barcoding and population genetic studies have revealed an unforeseen hidden diversity of cryptic species among microscopic marine benthos, otherwise exhibiting highly similar and simple morphologies. This has led to a paradigm shift, rejecting cosmopolitism of marine meiofauna until genetically proven and challenging the “Everything is Everywhere, but the environment selects” hypothesis that claims ubiquitous distribution of microscopic organisms. With phylogenetic and species delimitation analyses of worldwide genetic samples of the meiofaunal family Dinophilidae (Annelida) we here resolve three genera within the family and showcase an exceptionally broad, boreal, North Atlantic distribution of a single microscopic marine species with no obvious means of dispersal besides vicariance. With its endobenthic lifestyle, small size, limited migratory powers and lack of pelagic larvae, the broad distribution of Dinophilus vorticoides seems to constitute a “meiofaunal paradox”. This species feasts in the biofilm among sand grains, but also on macroalgae and ice within which it can likely survive long-distance rafting dispersal due to its varying lifecycle stages; eggs encapsulated in cocoons and dormant encystment stages. Though often neglected and possibly underestimated among marine microscopic species, dormancy may be a highly significant factor for explaining wide distribution patterns and a key to solving this meiofaunal paradox.

Highlights

DNA barcoding and population genetic studies have revealed an unforeseen hidden diversity of cryptic species among microscopic marine benthos, otherwise exhibiting highly similar and simple morphologies
‘Dinophilus taeniatus/vorticoides clade’ showed that it consists of minimally two separate phylogenetic entities (Table 1), thereby reflecting the presence of the two originally established species[32,33]
Molecular investigations of marine meiofauna generally argue against the ubiquity theorem (EiE)[20,21,22,23,24,25], and the few meiofaunal annelids proposed to have broad amphi-Atlantic distributions have all been disproven cosmopolitans when investigated genetically[7,23]

Summary

Introduction

DNA barcoding and population genetic studies have revealed an unforeseen hidden diversity of cryptic species among microscopic marine benthos, otherwise exhibiting highly similar and simple morphologies This has led to a paradigm shift, rejecting cosmopolitism of marine meiofauna until genetically proven and challenging the “Everything is Everywhere, but the environment selects” hypothesis that claims ubiquitous distribution of microscopic organisms. Unlike limno-terrestrial meiofauna, marine meiobenthos usually persist under stable abiotic conditions and are generally lacking dispersal mechanisms such as pelagic larvae or dormant, long-term viable stages With their small size, endobenthic lifestyle, limited migratory capabilities and lack of dispersal mechanisms, their supposed wide distribution indicated by morphological studies were a puzzle and coined as the “meiofauna www.nature.com/scientificreports paradox”[3,10,11]. These findings suggest that marine meiofauna can reveal interesting biogeographical patterns, potentially more significant than marine macrofauna with pelagic larva and complex dispersal strategies

Methods

Results

Conclusion