The ontogeny of asymmetry in echolocating whales.

Extreme asymmetry of the skull is one of the most distinctive traits that characterizes toothed whales (Odontoceti, Cetacea). The origin and function of cranial asymmetry are connected to the evolution of echolocation, the ability to use high-frequency sounds to navigate the surrounding environment. Although this novel phenotype must arise through changes in cranial development, the ontogeny of cetacean asymmetry has never been investigated. Here we use three-dimensional geometric morphometrics to quantify the changes in degree of asymmetry and skull shape during prenatal and postnatal ontogeny for five genera spanning odontocete diversity (oceanic dolphins, porpoises and beluga). Asymmetry in early ontogeny starts low and tracks phylogenetic relatedness of taxa. Distantly related taxa that share aspects of their ecology overwrite these initial differences via heterochronic shifts, ultimately converging on comparable high levels of skull asymmetry. Porpoises maintain low levels of asymmetry into maturity and present a decelerated rate of growth, probably retained from the ancestral condition. Ancestral state reconstruction of allometric trajectories demonstrates that both paedomorphism and peramorphism contribute to cranial shape diversity across odontocetes. This study provides a striking example of how divergent developmental pathways can produce convergent ecological adaptations, even for some of the most unusual phenotypes exhibited among vertebrates.

Wonky whales: the evolution of cranial asymmetry in cetaceans.

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.

Drivers of morphological evolution in the toothed whale jaw.

Toothed whales (odontocetes) emit high-frequency underwater sounds (echolocate)-an extreme and unique innovation allowing them to sense their prey and environment. Their highly specialized mandible (lower jaw) allows high-frequency sounds to be transmitted back to the inner ear. Echolocation is evident in the earliest toothed whales, but little research has focused on the evolution of mandibular form regarding this unique adaptation. Here, we use a high-density, three-dimensional geometric morphometric analysis of 100 living and extinct cetacean species spanning their ∼50-million-year evolutionary history. Our analyses demonstrate that most shape variation is found in the relative length of the jaw and the mandibular symphysis. The greatest morphological diversity was obtained during two periods of rapid evolution: the initial evolution of archaeocetes (stem whales) in the early to mid-Eocene as they adapted to an aquatic lifestyle, representing one of the most extreme adaptive transitions known, and later on in the mid-Oligocene odontocetes as they became increasingly specialized for a range of diets facilitated by increasingly refined echolocation. Low disparity in the posterior mandible suggests the shape of the acoustic window, which receives sound, has remained conservative since the advent of directional hearing in the aquatic archaeocetes, even as the earliest odontocetes began to receive sounds from echolocation. Diet, echolocation, feeding method, and dentition type strongly influence mandible shape. Unlike in the toothed whale cranium, we found no significant asymmetry in the mandible. We suggest that a combination of refined echolocation and associated dietary specializations have driven morphology and disparity in the toothed whale mandible.

The tempo of cetacean cranial evolution.

The evolution of cetaceans (whales and dolphins) represents one of the most extreme adaptive transitions known, from terrestrial mammals to a highly specialized aquatic radiation that includes the largest animals alive today. Many anatomical shifts in this transition involve the feeding, respiratory, and sensory structures of the cranium, which we quantified with a high-density, three-dimensional geometric morphometric analysis of 201 living and extinct cetacean species spanning the entirety of their ∼50-million-year evolutionary history. Our analyses demonstrate that cetacean suborders occupy distinct areas of cranial morphospace, with extinct, transitional taxa bridging the gap between archaeocetes (stem whales) and modern mysticetes (baleen whales) and odontocetes (toothed whales). This diversity was obtained through three key periods of rapid evolution: first, the initial evolution of archaeocetes in the early to mid-Eocene produced the highest evolutionary rates seen in cetaceans, concentrated in the maxilla, frontal, premaxilla, and nasal; second, the late Eocene divergence of the mysticetes and odontocetes drives a second peak in rates, with high rates and disparity sustained through the Oligocene; and third, the diversification of odontocetes, particularly sperm whales, in the Miocene (∼18-10 Mya) propels a final peak in the tempo of cetacean morphological evolution. Archaeocetes show the fastest evolutionary rates but the lowest disparity. Odontocetes exhibit the highest disparity, while mysticetes evolve at the slowest pace, particularly in the Neogene. Diet and echolocation have the strongest influence on cranial morphology, with habitat, size, dentition, and feeding method also significant factors impacting shape, disparity, and the pace of cetacean cranial evolution.

Supernumerary teeth observed in a live True's beaked whale in the Bay of Biscay.

Mesoplodont beaked whales are one of the most enigmatic mammalian genera. We document a pod of four beaked whales in the Bay of Biscay breaching and tail slapping alongside a large passenger ferry. Photographs of the animals were independently reviewed by experts, and identified as True's beaked whales (Mesoplodon mirus). This is the first conclusive live sighting of these animals in the north-east Atlantic, and adds information to previous sightings that are likely to have been M. mirus. Photographs of an adult male appears to show two supernumerary teeth posterior to the apical mandibular tusks. Whilst analysed museum specimens (n = 8) did not show evidence of alveoli in this location, there is evidence of vestigial teeth and variable dentition in many beaked whale species. This is the first such record of supernumerary teeth in True's beaked whales.