Masters of miniaturization: Convergent evolution among interstitial eukaryotes

Abstract

Marine interstitial environments are teeming with an extraordinary diversity of coexisting microeukaryotic lineages collectively called "meiofauna." Interstitial habitats are broadly distributed across the planet, and the complex physical features of these environments have persisted, much like they exist today, throughout the history of eukaryotes, if not longer. Although our general understanding of the biological diversity in these environments is relatively poor, compelling examples of developmental heterochrony (e.g., pedomorphosis) and convergent evolution appear to be widespread among meiofauna. Therefore, an improved understanding of meiofaunal biodiversity is expected to provide some of the deepest insights into the following themes in evolutionary biology: (i) the origins of novel body plans, (ii) macroevolutionary patterns of miniaturization, and (iii) the intersection of evolution and community assembly - e.g., "community convergence" involving distantly related lineages that span the tree of eukaryotes.

Biological adhesion of the flatworm Macrostomum lignano relies on a duo-gland system and is mediated by a cell type-specific intermediate filament protein

“…Therefore, most members of the meiofauna, including cnidarians, nematodes, annelids, gastrotrichs, and free-living flatworms developed mechanisms to temporarily attach to surfaces. These distantly related groups evolved structures for temporary adhesion, among other convergent morphologies, independently [33,69,70]. Within free-living flatworms several characters are shared with respect to their adhesive organs [33,35,36,38].…”

An Anatomical Description of a Miniaturized Acorn Worm (Hemichordata, Enteropneusta) with Asexual Reproduction by Paratomy

“…However, it is difficult to determine whether its many simple morphological traits should be interpreted as juvenile (from an arrest of growth due to progenetic origin) or just multiple losses (several uncoordinated evolutionary events) [47], [76]. Yet, taking into consideration the adaptive requirements of the interstitial milieu, favoring macroevolutionary changes [46], [47], [74], as well as the fact that enteropneust juveniles are already pre-adapted to this environment, it is likely that the origin of M. psammophilus gen. et sp. nov. is progenetic, as it has been proposed for other meiofaunal deuterostomes [26], [29].…”

“…Many others became miniaturized secondarily from macrofaunal ancestors [43]–[46]. The most popular evolutionary hypotheses explaining the many miniaturized forms in the interstitial environment, including meiofaunal ascidians and holothurians, is progenesis [26], [29], [47], based mainly on their resemblance to larval or juvenile stages of their macrofaunal relatives.…”

At the limits of a successful body plan - 3D microanatomy, histology and evolution of Helminthope (Mollusca: Heterobranchia: Rhodopemorpha), the most worm-like gastropod

“…Life in these minute spaces between sand grains constrains anatomy, and these taxa commonly show convergent morphologies with other meiofaunal organisms (called ‘meiofaunal syndrome’ herein). This involves a modified body plan with reduction or loss of pigmentation and body appendages (tentacles, shell, gill), an elongation of the body towards a worm-like shape, development of strong epidermal ciliation, adhesive abilities, and the repeated evolution of calcareous spicules as a presumed secondary ‘skeleton’ [6-10]. Other characters are the production of comparatively few but large eggs besides means of direct sperm transfer such as spermatophores or stylets, and the formation of additional ‘accessory’ ganglia in the nervous system.…”