4.8 Article

Alternating regimes of shallow and deep-sea diversification explain a species-richness paradox in marine fishes

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NATL ACAD SCIENCES
DOI: 10.1073/pnas.2123544119

关键词

fishes; deep sea; coral reefs; ecological filters; speciation rates

资金

  1. National Science Foundation
  2. [DEB-1556953]

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The disparity in species richness between shallow water and deep sea fish can be explained by alternating phases of shallow water diversification and deep-sea colonization and speciation. Shallow marine fish became highly diverse 100 million years ago during a period of warm temperatures and high sea level, while deep-sea colonization and speciation were favored during brief periods when cooling temperatures increased the efficiency of the ocean's carbon pump. Time-variable ecological filters limited the colonization from shallow to deep sea, maintaining higher species richness in shallow water.
The deep sea contains a surprising diversity of life, including iconic fish groups such as anglerfishes and lanternfishes. Still, >65% of marine teleost fish species are restricted to the photic zone <200 m, which comprises less than 10% of the ocean's total volume. From a macroevolutionary perspective, this paradox may be explained by three hypoth-eses: 1) shallow water lineages have had more time to diversify than deep-sea lineages, 2) shallow water lineages have faster rates of speciation than deep-sea lineages, or 3) shallow-to-deep sea transition rates limit deep-sea richness. Here we use phylogenetic comparative methods to test among these three non-mutually exclusive hypotheses. While we found support for all hypotheses, the disparity in species richness is better described as the uneven outcome of alternating phases that favored shallow or deep diversification over the past 200 million y. Shallow marine teleosts became incredibly diverse 100 million y ago during a period of warm temperatures and high sea level, sug-gesting the importance of reefs and epicontinental settings. Conversely, deep-sea coloni-zation and speciation was favored during brief episodes when cooling temperatures increased the efficiency of the ocean's carbon pump. Finally, time-variable ecological filters limited shallow-to-deep colonization for much of teleost history, which helped maintain higher shallow richness. A pelagic lifestyle and large jaws were associated with early deep-sea colonists, while a demersal lifestyle and a tapered body plan were typical of later colonists. Therefore, we also suggest that some hallmark characteristics of deep-sea fishes evolved prior to colonizing the deep sea.

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