From offshore to onshore: multiple origins of shallow-water corals from deep-sea ancestors.

Alberto Lindner,Clifford W Cunningham,Stephen D Cairns,Robert DeSalle

doi:10.1371/journal.pone.0002429

Alberto Lindner, Clifford W Cunningham + Show 2 more

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https://doi.org/10.1371/journal.pone.0002429

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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.

Highlights

The discovery of high species richness in the deep sea has led to a burst of hypotheses aiming to explain the origin and evolution of marine biodiversity [1,2,3]
The phylogeny shows that stylasterid corals originated and diversified in the deep sea, and invaded the shallow-water tropics three times (Figure 2)
Our results are the first demonstration of multiple invasions of tropical shallow waters by a major group of benthic marine invertebrates previously restricted to offshore, deep-water environments

Summary

Introduction

The discovery of high species richness in the deep sea has led to a burst of hypotheses aiming to explain the origin and evolution of marine biodiversity [1,2,3]. A shallow (onshore) to deep (offshore) evolutionary pattern has been invoked to explain the evolution of the Phanerozoic marine fauna [4], for abyssal taxa in general [5,6], and for the origin of hydrothermal vent communities [7]. Detailed analyses of the fossil record indicate that a shallow/onshore to deep/offshore pattern of evolution only holds for the initial diversification of the major groups of marine invertebrates, with ‘major’ referring to groups so distinct that they are assigned a taxonomic rank of ‘Order’ [14,15]. The fossil record indicates that important groups of animals that presently thrive in both deep and shallow waters—such as neogastropod mollusks and stylasterid corals—may have originated in deep offshore environments [14,15]

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