Cranial modularity drives phenotypic diversification and adaptive radiation of Antarctic icefishes

Modularity among traits is thought to drive morphological evolution and
diversification, with more modular species often showing greater disparity
and faster evolutionary rates. However, recent studies suggest this
pattern is not universal, as higher integration can sometimes be linked to
faster rates of evolution. In adaptive radiation, modularity likely
facilitates morphological divergence, but its specific role in trait
diversification within these events remains uncertain. Antarctic icefishes
(Perciformes: Notothenioidei) have undergone adaptive radiation in the
frigid Southern Ocean, yet the role of modularity in their craniofacial
evolution remains poorly understood. Emerging from a common ancestor 22
million years ago, these fishes developed unique morpho-physiological
adaptations, such as antifreeze glycoproteins, that contributed to their
evolutionary success, but the contribution of cranial modularity to their
diversification is still unexplored. Here, we analyze skull shape across
172 perciform species using micro-CT scanning and geometric morphometrics
to investigate the tempo and mode of skull evolution in 80 notothenioids
versus 92 perciform relatives. Notothenioids exhibit considerable cranial
shape diversity, with skull shapes ranging from short to long faces. Fast
rates of skull shape evolution occurred in smaller subclades following the
emergence of cranial elongation, a derived trait within notothenioids.
They also exhibit elevated evolutionary modularity relative to their
perciform relatives, with reduced covariation among skeletal elements over
time, likely corresponding with Miocene cooling events and the formation
of the Antarctic Circumpolar Current. We propose that greater phenotypic
modularity in notothenioid skulls represents a pivotal innovation,
facilitating their evolutionary response to new ecological opportunities
in the Antarctic.