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

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
hypotheses: 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 years ago during a
period of warm temperatures and high sea level, suggesting the importance
of reefs and epicontinental settings. Conversely, deep-sea colonization
and speciation were 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.