From Offshore to Onshore: Multiple Origins of Shallow-Water Corals from Deep-Sea Ancestors

Abstract

Shallow-water tropical reefs and the deep sea represent the two most diverse marine environments. Understanding the origin and diversification of this biodiversity is a major quest in ecology and evolution. The most prominent and well-supported explanation, articulated since the first explorations of the deep sea, holds that benthic marine fauna originated in shallow, onshore environments, and diversified into deeper waters. In contrast, evidence that groups of marine organisms originated in the deep sea is limited, and the possibility that deep-water taxa have contributed to the formation of shallow-water communities remains untested with phylogenetic methods. Here we show that stylasterid corals (Cnidaria: Hydrozoa: Stylasteridae)—the second most diverse group of hard corals—originated and diversified extensively in the deep sea, and subsequently invaded shallow waters. Our phylogenetic results show that deep-water stylasterid corals have invaded the shallow-water tropics three times, with one additional invasion of the shallow-water temperate zone. Our results also show that anti-predatory innovations arose in the deep sea, but were not involved in the shallow-water invasions. These findings are the first robust evidence that an important group of tropical shallow-water marine animals evolved from deep-water ancestors.

Temporary expansion to shelf depths rather than an onshore-offshore trend: the shallow-water rise and demise of the modern deep-sea brittle star family Ophiacanthidae (Echinodermata: Ophiuroidea)

“…Goldberg et al 2005). The present study adds to the growing body of evidence that modern shallow-water environments are not exclusively the result of in situ evolution but received considerable input from deep-sea invaders (Lindner et al 2008). Although, admittedly, adding the vertical migration component presents the risk of making palaeobiodiversity analyses exceedingly complex, straightforward exclusion of the potential contribution of deep-sea environments to shallow-water diversity is an oversimplification that is no longer tenable.…”

“…One of the very few authors to cast a comparably critical light on the shallow-water fossil record of an extant deep-sea group was Vörös (2005), who speculated that post-Palaeozoic smooth brachiopods invaded shallow environments as offshoots of stable deep-sea communities in times of suitable palaeoceanographic conditions. The potential of deep-sea groups to contribute to shallow-water diversity has recently been demonstrated by Lindner et al (2008), who showed that Recent shallow-water stylasterid corals evolved from deep-sea ancestors at least three times. Similar trends may thus be expected in other groups with both shallow and deep representatives.…”

“…2) middle shelf, approximately from 50 to 100 m, corresponding to the zone of occasional storm wave influence, reflected in the sedimentary record by thin distal tempestites; 100 m is generally considered as the maximum depth of storm wave action (Bottjer & Jablonski 1988;Lindner et al 2008); 3) deep shelf, approximately from 100 to 200 m, corresponding to the zone below maximum storm disturbance, reflected by the complete lack of tempestites and other wave-induced sedimentary features; often this zone still is within the photic zone, especially at low latitudes.…”

“…For example, using a worldwide phylogeny of stylasterid corals, Lindner et al (2008) showed that the group first appeared in a deep-water setting, extensively diversified in the deep sea and expanded to shallow-water habitats several times. Moura et al (2012) stressed the importance of the deep sea in generating and accumulating lineages of plumulariid hydrozoans that may occasionally invade coastal waters in the northeast Atlantic.…”

Distribution of cold-water corals in the Whittard Canyon, NE Atlantic Ocean

“…Corals are best known from shallow tropical seas, despite 465% of recorded coral species occurring below 50 m depth (Cairns, 2007;Lindner et al, 2008;Roberts et al, 2009). In contrast to their shallow-water counterparts, cold-water corals do not require light or high temperatures to survive in deep-waters because they do not have a symbiotic relationship with zooxanthellae (algae).…”