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. 2020 Jul 10;18(1):86.
doi: 10.1186/s12915-020-00805-4.

Wonky whales: the evolution of cranial asymmetry in cetaceans

Ellen J Coombs  1   2 , Julien Clavel  3 , Travis Park  4   5 , Morgan Churchill  6 , Anjali Goswami  7   4   8
Affiliations

Wonky whales: the evolution of cranial asymmetry in cetaceans

Ellen J Coombs et al. BMC Biol. .

Abstract

Background: 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. 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.

Results: In 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.

Conclusions: Early 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.

Keywords: Asymmetry; Cetaceans; Macroevolution; Morphometrics; Trait evolution.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Average radii per landmark (x̄ρland) for each taxon group. Landmarks superimposed onto a stylised skull which represents an average specimen for that group. Cooler yellows show less asymmetry, warmer oranges and reds show more asymmetry. The white landmarks are fixed reference landmarks (1-66) and therefore show no movement. From left to right: a the average landmark radii (x̄ρland) for terrestrial artiodactyls, b the average landmark radii for archaeocetes, c the average landmark radii for odontocetes, and d the average landmark radii for mysticetes. Landmarks on skulls a and d consist of pale yellows indicating low asymmetry. The landmarks on skull b are pale yellow, with darker yellows on the jugal, orbit, and rostrum indicating a higher level of asymmetry. Oranges and red landmarks in the nasal, posterior premaxilla, and posterior maxilla on skull c (the odontocete) indicate a high level of asymmetry. Skulls not to scale
Fig. 2
Fig. 2
Principal components 1 and 2 for full data set (n = 172, including 10 terrestrial artiodactyls). Circle size size reflects the sum radii in the skull for each specimen (∑pspec), with larger circles indicating higher ∑pspec. A morphospace labelled with a specimen key is provided in the Additional file 1: Fig. S5—principal components plot with PC1 and PC2 plotted for each specimen. Silhouettes are from Phylopic with credit attributed to Chris Huh and used under the Creative Commons Licence [30]
Fig. 3
Fig. 3
Time-calibrated phylogeny for sampled cetacean species indicating magnitude of cranial asymmetry (∑pspec). The labels highlight the following points: (1) archaeocetes, (2) mysticetes, (3) the origin of Neoceti (~ 39 Mya) [26], (4) early odontocetes including the xenorophids, (5) odontocetes, (6) the highly asymmetrical Platantista gangetica, (7) the highly asymmetrical monodontids, and (8) the highly asymmetrical Physeteroidea. The full data set (n = 162) is used. Phylogeny based on Lloyd and Slater [29]. Silhouettes are from Phylopic with credit attributed to Chris Huh and used under the Creative Commons Licence [30]
Fig. 4
Fig. 4
Reconstructed probability of shifts in cetacean cranial asymmetry. Reconstructed probability along each branch of the phylogeny under the assumption of relaxed Brownian motion with a Half-Cauchy distribution for the prior density of the rate scalar. Circles indicate a shift in the trait on either the branch or in the whole clade. The colour of the circle indicates the shift direction with red indicating forward shifts and blue indicating backwards shifts. The size of the circle indicates the probability of the shift occurring in that position in the clade with the largest circle (here, 0.750) indicating the highest probability of a shift occurring. The colour of the branch itself indicates posterior rates for that branch with red showing higher, increasing rates and blue showing lower, decreasing rates. The background rate is shown as grey. The asymmetry value is given as the sum of radii per specimen (∑pspec). A trace of the chain is provided in Additional file 1: Fig. S10—Gelman diagnostics for the two chains. Phylogeny based on Lloyd and Slater [29]
Fig. 5
Fig. 5
Reconstructed probability of jumps in the rate of cetacean cranial asymmetry. The model also predicts the number of jumps which may have occurred. The size of the circle indicates the probability of the jump occurring in that position in the clade with the largest circle (here, 0.750) indicating the highest probability of a jump occurring. The colour of the circle indicates the number of inferred jumps, where dark red = 5 and pale red = 1. The asymmetry value is given as the sum of radii per specimen (∑pspec). A trace of the chain is provided in Additional file 1: Fig. S10—Gelman diagnostics for the two chains. Phylogeny based on Lloyd and Slater [29]
Fig. 6.
Fig. 6.
Misalignment of mirrored landmarks when using the mirrorfill function on a specimen without bilateral symmetry. Landmarks mirrored in the geomorph package [90] on an asymmetric specimen. Note the incorrect mirroring of landmarks on the nasal and to a lesser extent on the lateral point of the maxilla near the orbit (circled) in this specific specimen. Inset shows the same skull with the landmarks correctly placed. Specimen is Delphinapterus leucas USNM 305071
Fig. 7.
Fig. 7.
123 landmarks (in black) placed on the dorsal (a) and ventral (b) of the skull. 9 landmarks were placed on the midline (for landmark details, see Additional file 1: Table S11–123 landmarks added to the entire surface of the skull). Specimen is Delphinapterus leucas USNM 305071
Fig. 8.
Fig. 8.
Visualisation of p (radii) from landvR showing asymmetry in the dolphin skull. Landmarks are placed on a stylised outline of a dolphin skull. The 3D surface scan of a dolphin skull (inset) is shown for orientation and is Lissodelphis borealis USNM 550188. The white spheres on the landvR output show the fixed landmarks (1–66) on the left-hand side (LHS) of the skull (looking down on the skull with the rostrum pointing north). The landmarks on the right-hand side (RHS) of the skull vary in colour depending on how much difference there is between a computer -mirrored landmark (Rn) (which assumes the skull is bilaterally symmetrical) and a manually placed landmark (Fn) (which accurately depicts asymmetry). The larger the difference between the computer -mirrored landmark and the manually placed landmark, the hotter the colour. The highest amount of asymmetry is shown in red and dark orange, less asymmetry is shown in pale orange and yellow. Note the red landmarks on the nasal and posterior premaxilla of this odontocete. The tails coming from each of the landmarks show how much and in which direction the landmarks have moved from where the computer mirrored them, to where the landmarks sit when manually placed
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