An anatomical description of a miniaturized acorn worm (hemichordata, enteropneusta) with asexual reproduction by paratomy.

Katrine Worsaae,Anders Hay-Schmidt,Sabrina Kaul-Strehlow,Gonzalo Giribet,Wolfgang Sterrer,Andreas Hejnol

doi:10.1371/journal.pone.0048529

Katrine Worsaae, Anders Hay-Schmidt + Show 4 more

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https://doi.org/10.1371/journal.pone.0048529

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Abstract

The interstitial environment of marine sandy bottoms is a nutrient-rich, sheltered habitat whilst at the same time also often a turbulent, space-limited, and ecologically challenging environment dominated by meiofauna. The interstitial fauna is one of the most diverse on earth and accommodates miniaturized representatives from many macrofaunal groups as well as several exclusively meiofaunal phyla. The colonization process of this environment, with the restrictions imposed by limited space and low Reynolds numbers, has selected for great morphological and behavioral changes as well as new life history strategies.Here we describe a new enteropneust species inhabiting the interstices among sand grains in shallow tropical waters of the West Atlantic. With a maximum body length of 0.6 mm, it is the first microscopic adult enteropneust known, a group otherwise ranging from 2 cm to 250 cm in adult size. Asexual reproduction by paratomy has been observed in this new species, a reproductive mode not previously reported among enteropneusts.Morphologically, Meioglossus psammophilus gen. et sp. nov. shows closest resemblance to an early juvenile stage of the acorn worm family Harrimaniidae, a result congruent with its phylogenetic placement based on molecular data. Its position, clearly nested within the larger macrofaunal hemichordates, suggests that this represents an extreme case of miniaturization. The evolutionary pathway to this simple or juvenile appearance, as chiefly demonstrated by its small size, dense ciliation, and single pair of gill pores, may be explained by progenesis. The finding of M. psammophilus gen. et sp. nov. underscores the notion that meiofauna may constitute a rich source of undiscovered metazoan diversity, possibly disguised as juveniles of other species.

Highlights

Hemichordata is a phylum of exclusively marine deuterostomes traditionally divided into the classes Pterobranchia and Enteropneusta [1,2,3,4], the latter including Ptychoderidae, Spengeliidae, Harrimaniidae and Torquaratoridae e.g., [4,5]
The finding of an enteropneust that remains meiofaunal during its entire life cycle - the smallest acorn worm known to date highlights the hidden diversity inhabiting the interstitial environment
Whereas various forms of asexual reproduction are found in Enteropneusta, this is the first example of paratomy

Summary

Introduction

Hemichordata is a phylum of exclusively marine deuterostomes traditionally divided into the classes Pterobranchia and Enteropneusta [1,2,3,4], the latter including Ptychoderidae, Spengeliidae, Harrimaniidae and Torquaratoridae e.g., [4,5]. Whereas all known acorn worms are solitary and range from 2– 250 cm in adult size, constituting part of the benthic macroinfauna, the sessile pterobranchs are colonial and consist of multiple minute zooids, each usually 0.5–5 mm long [9,10,11]. The origin of this deviant and small body plan is still poorly understood, especially if they nest among clades of macroscopic solitary acorn worms [6,7]. Most deuterostome species are macrofaunal, while microscopic, meiofaunal representatives of the deuterostome lineages are restricted to a handful of Tunicata (Chordata), Holothuroidea (Echinodermata), and, if truly deuterostome, most acoelomorphs [22,23,24,25,26,27,28,29,30]

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