Evolution of orbit size in toothed whales (Artiodactyla: Odontoceti)

Abstract

For many marine tetrapods, vision is important for finding food and navigating underwater, and eye size has increased to improve the capture of light in dim ocean depths. Odontocete whales, in contrast, rely instead on echolocation for navigation and prey capture. We tested whether the evolution of echolocation has influenced the orbit size, a proxy for eye size, and examined how orbit size evolved over time. We also assessed variation in orbit size amongst whales and tested how body size, diving ability, sound production, foraging habitat, and prey capture strategy influenced the orbit size using phylogenetic independent contrasts and phylogenetic ANOVAs. Using measurements of orbit length and bizygomatic width, we calculated proportional orbit size for 70 extant and 29 extinct whale taxa, with an emphasis on Odontoceti. We then performed ancestral character state reconstruction on a time‐calibrated composite phylogeny. Our analysis revealed that there was no shift in proportional orbit size from archaeocetes through stem odontocetes, indicating that the evolution of echolocation did not influence the orbit size. Proportional orbit size increased in Ziphiidae, Phocoenidae, and Cephalorhynchus. Proportional orbit size decreased in Balaenidae, Physeteridae, Platanistidae, and Lipotidae. Body size, diving ability, foraging environment, and prey capture strategy had a significant influence on orbit size, but only without phylogenetic correction. An increase in orbit size is associated with deep diving behavior in beaked whales, while progenesis and retention of juvenile features into adulthood explain the pattern observed in Phocoenidae and Cephalorhynchus. Decrease in proportional orbit size is associated with adaptation toward murky freshwater environments in odontocetes and skim feeding in balaenids. Our study reveals that the evolution of echolocation had little effect on orbit size, which is variable in whales, and that adaptation for different feeding modes and habitat explains some of this variance.

New Skeletons of the Ancient Dolphin Xenorophus sloanii and Xenorophus simplicidens sp. nov. (Mammalia, Cetacea) from the Oligocene of South Carolina and the Ontogeny, Functional Anatomy, Asymmetry, Pathology, and Evolution of the Earliest Odontoceti

“…No change in orbit size was apparent at the base of Odontoceti, which is reinforced by the results here showing that Xenorophidae bear relatively similar orbit sizes and angles to archaeocetes and some toothed mysticetes. Large orbits in small cetaceans (e.g., Phocoenidae, Cephalorhynchus, and probably Parapontoporia) are likely driven by paedomorphosis [53]. These authors likewise found a similar link between small eyes and murky freshwater habitats, and also highlighted a slight increase in orbit size within the deep-diving Ziphiidae [53].…”

“…Large orbits in small cetaceans (e.g., Phocoenidae, Cephalorhynchus, and probably Parapontoporia) are likely driven by paedomorphosis [53]. These authors likewise found a similar link between small eyes and murky freshwater habitats, and also highlighted a slight increase in orbit size within the deep-diving Ziphiidae [53].…”

“…Coombs et al [52] indicated that a major shift in odontocete skull asymmetry occurs within the clade, likely corresponding to the initial evolution of echolocation [3,4,19]. In a study of orbit size evolution within odontocetes, Churchill and Baltz [53] found that xenorophids have a relatively similar orbit size to basilosaurid whales, indicating minimal evolution of vision across the basilosaurid-odontocete transition. Owing to their already derived cranial morphology, basal position within Odontoceti, and rapid divergence from Basilosauridae, Coombs et al [54] found some of the highest evolutionary rates of skull evolution amongst cetaceans within the Xenorophidae, part of a rapid radiation of early Neoceti.…”

“…Chaeomysticetes, on the other hand, generally had more laterally facing orbits (orbital angle 65-90 • ) that were smaller (relative orbit size 27-8% BZW). A recent and more elaborate study by Churchill and Baltz [53] investigated the interplay between orbit size evolution and the origin of echolocation within the Odontoceti. No change in orbit size was apparent at the base of Odontoceti, which is reinforced by the results here showing that Xenorophidae bear relatively similar orbit sizes and angles to archaeocetes and some toothed mysticetes.…”

Evolutionary trends in the elasmobranch neurocranium

“…Herein correlations between neurocranium shape and ecology in Elasmobranchii are restricted to three broad categories (depth, 'water conditions' and latitude), with most other correlations being lost when taking phylogeny into account (Table 1; Table 2; Supplementary Table S4). Whilst the absence of rate differences between modules in the selachimorph neurocranium (Supplementary Table S5; Supplementary Table S6) provides rudimentary evidence of natural selection across the braincase [53][54], this does not match observed patterns of ecological signal, which appear to differ signi cantly between different regions of the braincase (Table 2). As mentioned previously, the orbit and the rostrum were found to be the most variable regions of the neurocranium, which is notable given the hypothesised functional importance of these structures (Table 2; Supplementary Table S7) [32][33][34].…”