The ontogeny of asymmetry in echolocating whales

Abstract

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.

Testing heterochrony: Connecting skull shape ontogeny and evolution of feeding adaptations in baleen whales

“…As shown in previous studies of Cetacea (e.g., Lanzetti et al, 2022), skull allometry can vary significantly across taxa. Therefore, we first tested differences in allometry among genera and obtained taxon-specific regression parameters.…”

“…Alterations in location and timing of gene expression have also been implicated in the evolution of homodont dentition in Odontoceti and in the growth of baleen during the prenatal development of modern Mysticeti (Armfield et al, 2013; Thewissen et al, 2017). Heterochrony on a broader, phenotypic level has also been found to have had a strong impact on the phylogeny and diversification of Odontoceti, especially in porpoises and at least one dolphin genus ( Cephalorhynchus ; e.g., Galatius, 2010), including by influencing their level of skull asymmetry and related hearing adaptations (Lanzetti et al, 2022).…”

Testing heterochrony: Connecting skull shape ontogeny and evolution of feeding adaptations in baleen whales

“…As shown in previous studies of Cetacea (e.g. Groves et al, 2021;Lanzetti et al, 2022), skull allometry can vary significantly across taxa. Therefore, we first tested for differences in allometry among genera and obtained taxon-specific regression parameters.…”

“…We again used the ‘procD.lm’ functions, adding genus as a covariate, to reconstruct the separate allometric regressions, and tested pairwise differences between the slopes using ‘pairwise’ in the package ‘RRPP’ v. 1.1.2 (Collyer and Adams, 2021). We then used these extracted regression parameters (slopes and intercepts) to estimate the ancestral allometries and reconstruct the polarities of any heterochronic shifts (Alberch et al, 1979) following Morris et al (2019) and Lanzetti et al (2022). Using the phylogeny from McGowen et al (2020), we calculated ancestral slope and intercepts parameters for the nodes with the ‘fastAnc’ function and mapped the character changes on the tree with the ‘contMap’ function, both implemented in ‘phytools’ v. 1.0 (Revell, 2012).…”

“…Alterations in location and timing of gene expression have also been implicated in the evolution of homodont dentition in Odontoceti and in the growth of baleen during the prenatal development of modern Mysticeti (Armfield et al, 2013; Thewissen et al, 2017). Heterochrony on a broader, phenotypic level has also been found to have had a strong impact on the phylogeny and diversification of Odontoceti, especially in porpoises and at least one dolphin genus ( Cephalorhynchus ) (Galatius and Kinze, 2003; Galatius, 2010; Galatius et al, 2011), including by influencing their level of skull asymmetry and related hearing adaptations (Lanzetti et al, 2022).…”