The evolution of annelids reveals two adaptive routes to the interstitial realm

Abstract

Many animals permanently inhabit the marine interstitium, the space between sand grains [1, 2]. Different evolutionary scenarios may explain the existence of interstitial animals [3, 4]. These scenarios include (1) that the interstitial realm is the ancestral habitat of bilaterians [5, 6], (2) that interstitial taxa evolved from larger ancestors by miniaturization, or (3) progenesis [3]. The first view mirrors the former hypothesis that interstitial annelids, called archiannelids, were at the base of the annelid radiation [7]. Based on morphological data, however, progenesis is generally favored for interstitial annelids today [3, 4, 8]. Herein, our phylogenomic approach revealed that interstitial archiannelids are robustly placed into two groups nested within the annelid tree. Evolution of the first group comprising among others Dinophilidae is best explained by progenesis. In contrast, the second group comprising Protodrilida and Polygordiidae appears to have evolved by stepwise miniaturization adapting from coarser to finer sediments. Thus, in addition to progenesis [3, 4], miniaturization, thought to be too slow for an adaptation to the interstitium [3], is an important second route allowing adaptation to interstitial environments. Both progenesis and miniaturization should be considered when investigating evolution of interstitial taxa [1, 3].