Ecophysiological steps of marine adaptation in extant and extinct non‐avian tetrapods

Abstract

Marine reptiles and mammals are phylogenetically so distant from each other that their marine adaptations are rarely compared directly. We reviewed ecophysiological features in extant non-avian marine tetrapods representing 31 marine colonizations to test whether there is a common pattern across higher taxonomic groups, such as mammals and reptiles.Marine adaptations in tetrapods can be roughly divided into aquatic and haline adaptations, each of which seems to follow a sequence of three steps. In combination, these six categories exhibit five steps of marine adaptation that apply across all clades except snakes: Step M1, incipient use of marine resources; Step M2, direct feeding in the saline sea; Step M3, water balance maintenance without terrestrial fresh water; Step M4, minimized terrestrial travel and loss of terrestrial feeding; and Step M5, loss of terrestrial thermoregulation and fur/plumage. Acquisition of viviparity is not included because there is no known case where viviparity evolved after a tetrapod lineage colonized the sea. A similar sequence is found in snakes but with the haline adaptation step (Step M3) lagging behind aquatic adaptation (haline adaptation is Step S5 in snakes), most likely because their unique method of water balance maintenance requires a supply of fresh water. The same constraint may limit the maximum body size of fully marine snakes.Steps M4 and M5 in all taxa except snakes are associated with skeletal adaptations that are mechanistically linked to relevant ecophysiological features, allowing assessment of marine adaptation steps in some fossil marine tetrapods. We identified four fossil clades containing members that reached Step M5 outside of stem whales, pinnipeds, sea cows and sea turtles, namely Eosauropterygia, Ichthyosauromorpha, Mosasauroidea, and Thalattosuchia, while five other clades reached Step M4: Saurosphargidae, Placodontia, Dinocephalosaurus, Desmostylia, and Odontochelys. Clades reaching Steps M4 and M5, both extant and extinct, appear to have higher species diversity than those only reachingSteps M1 to M3, while the total number of clades is higher for the earlier steps. This suggests that marine colonizers only diversified greatly after they minimized their use of terrestrial resources, with many lineages not reaching these advanced steps.Historical patterns suggest that a clade does not advance to Steps M4 and M5 unless these steps are reached early in the evolution of the clade. Intermediate forms before a clade reached Steps M4 and M5 tend to become extinct without leaving extant descendants or fossil evidence. This makes it difficult to reconstruct the evolutionary history of marine adaptation in many clades. Clades that reached Steps M4 and M5 tend to last longer than other marine tetrapod clades, sometimes for more than 100 million years.

Spinosaurusis not an aquatic dinosaur

“…All large-bodied secondarily aquatic vertebrates — both extant (e.g., sea turtles, sirenians, seals, whales) and extinct (e.g., protostegid turtles, ichthyosaurs, metriorhynchoid crocodylomorphs, plesiosaurs) - are marine; none have been shown to live in both saltwater and freshwater habitats. Secondarily aquatic vertebrates that live in freshwater habitats ( Evers and Benson, 2019 ; Motani and Vermeij, 2021 ). Secondarily aquatic vertebrates that live in freshwater habitats have marine antecedents and are all small-bodied, such as river dolphins (<2.5 m length; Hamilton et al (2001 )), small lakebound seals (<2 m; Fulton and Strobeck (2010 )), the riverbound Amazonian manatee (<2.5 m; Guterres-Pazin (2014 )), and a few mosasaurs and plesiosaurs of modest body size ( Gao et al, 2016 ).…”

“…The large body size of S. aegyptiacus and antecedent species such as S. tenerensis also mitigates against an aquatic interpretation for the former, as it would constitute the only instance among vertebrates where the evolution of a secondarily aquatic species occurred at body size greater than 2-3 m. All other large-bodied secondarily aquatic vertebrates (e.g., ichthyosaurs, plesiosaurs, metriorhynchoid crocodylomorphs, protostegid turtles, mosasaurs, sirenians, whales) transitioned to an aquatic lifestyle at small body size, radiating subsequently within the marine realm to larger body size ( Domning, 2000 ; Polcyn et al, 2014 ; Moon and Stubbs, 2020 ; Motani and Vermeij, 2021 ; Thewissen et al, 2009 ).…”

Trends of avian locomotion in water – an overview of swimming styles

“…During the history of Earth, several primarily terrestrial lineage of tetrapods have returned to the water and adapted on different levels to live in an aquatic environment (Kelley & Pyenson 2015, Motani & Vermeij 2021. Some of these transitions could be connected to the colonisation of aquatic environments during the recovery after devastating mass extinctions, however, most of these events are scattered through geological time and probably were driven by the available food sources and high productivity of aquatic habitats (Vermeij & Motani 2018).…”

“…Some of these transitions could be connected to the colonisation of aquatic environments during the recovery after devastating mass extinctions, however, most of these events are scattered through geological time and probably were driven by the available food sources and high productivity of aquatic habitats (Vermeij & Motani 2018). The aquatic adaptation of different clades to similar physical parameters and challenges has resulted in similar anatomical solutions and thus, convergent forms in many cases (Lindgren et al 2010, Motani & Vermeij 2021, Gutarra & Rahman 2022. The waters of the Mesozoic were ruled by several clades of marine reptiles (such as sauropterygians, ichthyopterygians, mosasaurs, etc.…”

“…From the beginning of the Cenozoic, the radiation of aquatic mammals (such as pinnipeds, cetaceans, sirenians, etc.) has begun (Uhen 2007, Kelley & Pyenson 2015, Motani & Vermeij 2021. Nowadays, aquatic birds represent important components of both marine and freshwater ecosystems.…”