Abstract
BackgroundUnlike most mammals, toothed whale (Odontoceti) skulls lack symmetry in the nasal and facial (nasofacial) region. This asymmetry is hypothesised to relate to echolocation, which may have evolved in the earliest diverging odontocetes. Early cetaceans (whales, dolphins, and porpoises) such as archaeocetes, namely the protocetids and basilosaurids, have asymmetric rostra, but it is unclear when nasofacial asymmetry evolved during the transition from archaeocetes to modern whales. We used three-dimensional geometric morphometrics and phylogenetic comparative methods to reconstruct the evolution of asymmetry in the skulls of 162 living and extinct cetaceans over 50 million years.ResultsIn archaeocetes, we found asymmetry is prevalent in the rostrum and also in the squamosal, jugal, and orbit, possibly reflecting preservational deformation. Asymmetry in odontocetes is predominant in the nasofacial region. Mysticetes (baleen whales) show symmetry similar to terrestrial artiodactyls such as bovines. The first significant shift in asymmetry occurred in the stem odontocete family Xenorophidae during the Early Oligocene. Further increases in asymmetry occur in the physeteroids in the Late Oligocene, Squalodelphinidae and Platanistidae in the Late Oligocene/Early Miocene, and in the Monodontidae in the Late Miocene/Early Pliocene. Additional episodes of rapid change in odontocete skull asymmetry were found in the Mid-Late Oligocene, a period of rapid evolution and diversification. No high-probability increases or jumps in asymmetry were found in mysticetes or archaeocetes. Unexpectedly, no increases in asymmetry were recovered within the highly asymmetric ziphiids, which may result from the extreme, asymmetric shape of premaxillary crests in these taxa not being captured by landmarks alone.ConclusionsEarly ancestors of living whales had little cranial asymmetry and likely were not able to echolocate. Archaeocetes display high levels of asymmetry in the rostrum, potentially related to directional hearing, which is lost in early neocetes—the taxon including the most recent common ancestor of living cetaceans. Nasofacial asymmetry becomes a significant feature of Odontoceti skulls in the Early Oligocene, reaching its highest levels in extant taxa. Separate evolutionary regimes are reconstructed for odontocetes living in acoustically complex environments, suggesting that these niches impose strong selective pressure on echolocation ability and thus increased cranial asymmetry.
Highlights
Unlike most mammals, toothed whale (Odontoceti) skulls lack symmetry in the nasal and facial region
Fahlke et al [16] hypothesised that basilosaurids and protocetids have cranial asymmetry thought to be linked to aquatic directional hearing with the most conspicuous asymmetry occurring in the rostrum [15, 16]
Cranial asymmetry across cetaceans Comparing the sum radii (Σρspec) for each specimen in our data set, we found that odontocetes, especially the monodontids, physeterids, and kogiids, are the most asymmetrical of the cetaceans (Table 1)
Summary
Unlike most mammals, toothed whale (Odontoceti) skulls lack symmetry in the nasal and facial (nasofacial) region This asymmetry is hypothesised to relate to echolocation, which may have evolved in the earliest diverging odontocetes. Asymmetry in odontocetes is always unidirectional, with a posterior and sinistral shift in the bones, linked to the hypertrophied melon, phonic lips, and nasal sacs, all of which are associated with high-frequency sound production and echolocation [16, 17] Most of this asymmetry appears in the dorsal opening of the nares [14, 15, 18] and appears to be correlated with the degree of elevation in the cranial vertex [11]. Species with high cranial vertices such as physeterids, kogiids, and ziphiids tend to have the most asymmetrical crania, likely because a functional component of asymmetry pertains to soft facial anatomy and drives evolution of the underlying bony structures [11]
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