Genes lost during the transition from land to water in cetaceans highlight genomic changes involved in aquatic adaptations

Abstract

The transition from land to water in whales and dolphins (cetaceans) was accompanied by remarkable anatomical, physiological and behavioral adaptations. To better understand the genomic changes that occurred during this transition, we systematically screened for protein-coding genes that were inactivated in the ancestral cetacean lineage. We discovered genes whose loss is likely beneficial for cetaceans by reducing the risk of thrombus formation during diving (F12, KLKB1), improving the fidelity of oxidative DNA damage repair (POLM), and protecting from oxidative stress-induced lung inflammation (MAP3K19). Additional gene losses may reflect other diving-related adaptations, such as enhanced vasoconstriction during the diving response (mediated by SLC6A18) and altered pulmonary surfactant composition (SEC14L3), while loss of SLC4A9 relates to a reduced need for saliva in aquatic environments. Finally, the complete loss of melatonin synthesis and receptor genes (AANAT, ASMT, MTNR1A/B) may have been a precondition for the evolution of unihemispheric sleep. Our findings suggest that some genes lost in the ancestral cetacean lineage may have been involved in adapting to a fully-aquatic lifestyle.

Natural Tolerance to Ischemia and Hypoxemia in Diving Mammals: A Review

“…Two peroxiredoxin gene families (PRDX1 and PRDX3) are also expanded in cetacean lineages (Yim et al, 2014; Zhou et al, 2018), suggesting an augmented capacity for redox signaling and antioxidant protection (Perkins et al, 2015). Moreover, an inactivating mutation in the cetacean gene encoding Polμ, a polymerase with low fidelity in repairing oxidative DNA damage, suggests that reliance on a higher fidelity polymerase (Polλ) may confer tolerance to oxidative damage (Pryor et al, 2015; Huelsmann et al, 2019). In cetaceans, contracted gene families involved in the acute inflammatory response and repair of lipid peroxidation support physiological data in deep-diving pinnipeds that suggest that these animals may have evolved mechanisms to cope with ischemic inflammation associated with diving (Tift et al, 2014; Bagchi et al, 2018; Meyer et al, 2018; Zhou et al, 2018).…”

Convergent vomeronasal system reduction in mammals coincides with convergent losses of calcium signalling and odorant‐degrading genes

“…In this context, the inactivation of protein‐coding, also referred to as gene loss, has recently received more and more attention (Albalat & Canestro, ; Sharma et al, ). The inactivation or loss of protein‐coding genes reflects adaptations to diverse ecological niches including the change to a subterranean or aquatic habitat (Chikina, Robinson, & Clark, ; Ehrlich et al, ; Huelsmann et al, ; Kishida, Kubota, Shirayama, & Fukami, ; Lopes‐Marques et al, ; Nery, Arroyo, & Opazo, ; Partha et al, ; Prudent, Parra, Schwede, Roscito, & Hiller, ; Sharma et al, ) and various nutrition strategies that range from carnivory, herbivory, insectivory to frugivory (Hecker, Sharma, & Hiller, ; Huelsmann et al, ; Jiang et al, ; Kim et al, ; Liu et al, ; Lopes‐Marques et al, ; Sharma et al, ). Hence, studying the inactivation of protein‐coding genes constitutes a promising approach to gain further insights into evolutionary ecology.…”

The dopamine receptor D5gene shows signs of independent erosion in toothed and baleen whales

“…Reductive episodes have been widely documented across the tree of life contributing to organismal divergence and physiological and morphological adaptation to environmental cues (Albalat & Cañestro, 2016; Braun, 2003; Jeffery, 2009; Olson, 1999). In agreement, gene loss mechanisms seem pervasive in lineages that endured drastic habitat transitions in the course of evolution, such as Cetacea, entailing niche-specific adaptations (Huelsmann et al, 2019; Lachner et al, 2017; Lopes-Marques et al, 2018; Lopes-Marques et al, 2019a; McGowen, Gatesy & Wildman, 2014; Nery, Arroyo & Opazo, 2014; Sharma et al, 2018; Strasser et al, 2015). Thus, our findings suggest that these species are natural KOs for this dopamine receptor and might offer valuable insights into the mechanisms of some forms of essential hypertension.…”