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

• Published in: Journal of anatomy 2021-12, Vol.239 (6), p.1419-1437
• Main Authors: Churchill, Morgan, Baltz, Colin
• Format: Article
• Language: English
• Subjects: Animals; Artiodactyla; Body size; Cephalorhynchus; Cetacea; Diving; Diving behavior; Dolphins; Echolocation; Evolution; Feeding behavior; Freshwater environments; Odontoceti; Original Paper; Original Papers; Phocoenidae; Phylogenetics; Phylogeny; Prey; Sound production; Whales; Ziphiidae
• ISSN: 0021-8782; 1469-7580
• DOI: 10.1111/joa.13522

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. Ancestral character state reconstruction of orbit size shows that orbit size was not influenced by the evolution of echolocation in odontocetes. However some lineages show increases in orbit size consistent with deep‐diving behavior and paedomorphosis, while other lineages show decreases in orbit size, consistent with adaptation to freshwater habitats.