Distinct evolutionary signatures underlie body shape diversity across deep-sea habitats

The deep sea is known for extreme biological conditions such as high
pressure, little to no solar light, and cold temperatures. Despite these
challenges, deep-sea fishes have been shown to have higher body shape
diversity than shallow-sea relatives. An open question is whether
different habitats within the deep sea differentially contribute to this
surprising phenotypic diversity. Here, we explore the joint effects of two
major environmental dimensions in marine ecosystems, the benthic-pelagic
axis and ocean depth, on phenotypic diversification in teleost fishes.
Using measurements of body shape across nearly 3,000 species, we found
that increasing ocean depth generally shifted axes of phenotypic evolution
and promoted diversification for benthic, demersal, and pelagic fishes
alike. However, body shape diversity and rates of body shape evolution did
not scale evenly across these habitat divisions. For benthic fishes, the
rate increased more strongly than diversity with ocean depth, while the
reverse was true for pelagic fishes. Analyses of historical transition
rates showed that routes to colonizing deep-pelagic habitats have been
more variable than those for colonizing deep-benthic habitats, suggesting
that independent invasions from different sources may help explain the
diversity of deep-pelagic fishes without invoking high evolutionary rates.
Relaxed selection on body shape may also explain this diversity, as
suggested by the extreme range of forms found in the deep pelagic,
coinciding with an elongation axis shared by all deep-sea fishes. Overall,
our results reveal a mosaic of pathways through which body plan diversity
has accumulated across a large vertebrate radiation, underscoring the
importance of considering finer-scale habitat variation in broad-scale
evolutionary studies.