Bathymetric evolution of black corals through deep time

Abstract

Deep-sea lineages are generally thought to arise from shallow-water ancestors, but this hypothesis is based on a relatively small number of taxonomic groups. Anthozoans, which include corals and sea anemones, are significant contributors to the faunal diversity of the deep sea, but the timing and mechanisms of their invasion into this biome remain elusive. Here, we reconstruct a fully resolved, time-calibrated phylogeny of 83 species in the order Antipatharia (black coral) to investigate their bathymetric evolutionary history. Our reconstruction indicates that extant black coral lineages first diversified in continental slope depths (∼250-3000 m) during the early Silurian (∼437 millions of years ago (Ma)) and subsequently radiated into, and diversified within, both continental shelf (less than 250 m) and abyssal (greater than 3000 m) habitats. Ancestral state reconstruction analysis suggests that the appearance of morphological features that enhanced the ability of black corals to acquire nutrients coincided with their invasion of novel depths. Our findings have important conservation implications for anthozoan lineages, as the loss of 'source' slope lineages could threaten millions of years of evolutionary history and confound future invasion events, thereby warranting protection.

Keywords: abyss; adaptations; antipatharia; shelf; slope; ultraconserved elements.

Figure 1.

Time-calibrated phylogeny of the Antipatharia with ancestral character states of depth. BEAST2-dated phylogeny constructed from 25 clock-like loci. Depth ranges for each depth zone are as follows: shelf (0–250 m), slope (250–3000 m) and abyss (greater than 3000 m). Posterior probability values at each node are greater than 0.95 unless indicated by ‘*’. Tree is scaled to time in millions of years. Mass extinction events are shown (dashed vertical lines). Ancestral state reconstructions for depth are illustrated with pie diagrams at nodes; (O, Ordovician; S, Silurian; D, Devonian; C, Carboniferous; P, Permian; T, Triassic; J, Jurassic; K, Cretaceous; P, Palaeogene, N, Neogene).

Figure 2.

Morphological features of the Antipatharia. Myriopathes sp. colony showing flabellate and pinnulate characteristics (a), Antipathes sp. colony showing bramble and non-pinnulate characteristics (b), Antipathes sp. colony showing branched and non-pinnulate characteristics (c), Schizopathes affinis showing pinnulate branches and a basal hook, enlarged in inset (d), and Heteropathes americana showing a curved stem and pinnulate branches that form a wind-tunnel appearance (e).