One of the great transformations in evolution of vertebrates has been the return to the aquatic environment after the conquest of terrestrial ecosystems. With structural and physiological characteristics adapted to function on land, the various non-piscine taxa had to modify these characteristics to perform in water. Secondary aquatic vertebrates successfully transformed mechanisms for feeding, locomotion, osmoregulation, and sensory systems to function and thrive in an aqueous environment. This symposium emphasized the changes that had to be acquired to operate in the water with morphologies previously evolved to function on land. It brought together researchers working on different aspects of functional biology and on various taxa in order to illustrate the diversity in the required adaptations: the numerous convergences as well as the specific adaptive traits. The collection of talks, posters, and of the contributions to this special volume highlights recent advances in the understanding of the functional adaptations associated to secondary adaptation to an aquatic lifestyle in vertebrates.
In the course of vertebrate evolution, there have been a number of great transformations (e.g., acquisition of jaws, amniote egg, limbs, wings, endothermy) that have directed the trajectory of various lineages (Carroll 1997; Dial et al. 2015). Among the key transformations are the adaptations to specific environments, and notably the movement of vertebrates from water onto land (Ashley-Ross et al. 2013; Zimmer 2014). The changes associated with evolution of fins to legs and the departure from an obligate aquatic existence have been the hallmark of evidence for evolutionary change (Clack 2012). This transformation has emphasized the importance of homology. Indeed, fossils have been traced through common descent, supporting a singular evolutionary event that led to the diverse assemblage of vertebrate tetrapods. However, the converse event of the secondary invasion of the aquatic realm by reptiles, birds, and mammals has emphasized not only homology but homoplasy. Indeed, there are strong selective pressures that inflict functional constraints on whole-organism performance. These constraints led to the acquisition of numerous convergences that were imposed by the aquatic physical environment (Mazin and de Buffrénil 2001; Thewissen and Nummela 2008).
The aim of this symposium was to focus on vertebrate secondary adaptations to an aquatic life, which is a major theme in vertebrate evolutionary biology. The change from terrestrial to aquatic lifestyles required a combination of morphological, physiological, and behavioral adaptations, with modifications in reproduction, sensory organs, locomotor systems, etc. This ecological shift occurred in various taxa exhibiting different phylogenetic backgrounds and diverse body plans (Carroll, 1985; Houssaye 2009). Beyond convergences, different solutions evolved to common problems associated with an aquatic existence. Convergences of highly derived aquatic vertebrates have been the quintessential examples of evolutionary transition, like the similar (thunniform) swimming mode and morphological design exemplified by tuna fishes, ichthyosaurs, and cetaceans (Howell, 1930; Braun and Reif, 1985). However, a wide range of adaptations exist that reflect compromises to the degree of adaptation between semi-aquatic and fully aquatic species (e.g., shallow water versus open sea; ambulatory versus swimming locomotion; surface swimming, shallow or deep diving).
This symposium proposed to focus on the functional adaptations driving the phenotypic variation and ecological diversity in semi-aquatic and aquatic taxa. These fossil and extant vertebrate taxa include amphibians (because of their biphasic life history; Carroll, 2007), reptiles, birds, and mammals. The symposium presented different approaches to discuss the morphological evolution in feeding and sensory adaptations, osmoregulation, locomotion, and osteology.
Feeding and sensory adaptations
The ecological shift from land to water imposed changes in sensory systems, foraging strategy, and feeding mode.
Sensory adaptations include changes in, for example, electroreception for electrolocation and electrocommunication, olfaction (vomeronasal system), balance (spatial orientation, movement perception), vision (cornea curvature, retinal topography), and hearing (acoustics, ear anatomy) (Thewissen and Nummela 2008). Ketten (2016) discussed the underwater sound reception mechanisms in various aquatic amniotes. She uses computerized tomography (CT) and magnetic resonance imaging (MRI) to map densities of tissues associated with the outer, middle, and inner ears of sea turtles, sea birds, pinnipeds, odontocetes, and mysticetes. Her study reveals the occurrence of similar bundles of fatty tissues contacting the tympanum in all examined taxa suggesting the parallel evolution of similar soft-tissues involved in underwater sound conveyance to the middle and inner ear.
Feeding in water is challenging for organisms originally adapted to a terrestrial existence. Associated with different biomechanical systems, there are naturally different types of prey capture (suspension feeding, suction feeding, or jaw prehension), and ingestion (Schwenk and Rubega 2005). Heiss (2016) presented the phenotypic plasticity in feeding mode associated with the multiphasic (aquatic versus terrestrial) lifestyle of salamanders (Amphibia): He highlighted the shift from suction feeding in water to tongue prehension for terrestrial prey capture and how the associated changes prevent suction feeding abilities. Though snakes do not use suction feeding, Segall and collaborators (2016) showed that the aquatic milieu constrained head shape evolution in snakes (Squamata), engendering morphological convergences through the numerous independent reinvasions of water. Their observations validate their predictions based on biomechanical models and show a narrower anterior part of the head and posteriorly located nostrils and eyes in aquatic snakes, as compared to their terrestrial relatives. Domning (2016) illustrated the very diverse feeding modes and associated skull and tooth morphologies observed in Sirenia (Mammalia). Indeed, through their evolutionary history, these aquatic plant feeders resorted to various feeding strategies, such as selective browsing, less selective grazing, rhizivory, algivory, durophagy, and even hard food crushing. Goodall and Purnell (2016) illustrated the dietary transitions accompanying cetacean origin through 3D texture analysis of tooth microwear. Based on correlation between tooth microtextures and diet in modern aquatic mammals, they analyzed the shift from terrestrial omnivory/herbivory to aquatic piscivory/carnivory in archaeocete whales and showed a complex picture of dietary evolution in these taxa. A. and collaborators also analyzed cetacean feeding evolution with regard to the origin of baleen and filter feeding in mysticetes (Berta et al. 2016). They resorted to morphological, molecular and isotopic data to analyze this transition in diet and environment, and highlighted the ontogenetic changes in skull development, resorption of fetal dentition, and growth of baleen.
Brischoux (2016) elucidated the osmoregulation challenge associated with a marine existence by discussing hypernatremia in marine snakes and the evolution of an euryhaline physiology. He highlighted a relatively high physiological tolerance to hypernatremia in all snakes, compared to other marine tetrapods, and suggested that high tolerance to hypernatremia constitutes an important step in the evolution of an euryhaline physiology that may have preceded the evolution of salt glands.
Locomotion in a dense and viscous medium, such as water, imposes strong hydrodynamic demands on the musculoskeletal system by implying greater forces and specialized locomotor kinematics and muscle activation patterns (Gillis and Blob 2001; Herrel et al. 2012). Thus, drag reduction, increase in propulsive force production and buoyancy control are the main constraints driving adaptive changes required to improve locomotor performance and stability (Fish and Stein 1991; Fish 2000, 2002).
Fish discussed the evolution of advanced swimming modes, through enhanced locomotor performance (increased speed, drag reduction, improved thrust output, and increased manoeuvrability) based on biomechanical models. He showed that recently discovered fossils validate much of a previous model built for mammals (Fish 2000). He went on to propose a biomechanical model for birds to describe the evolution of specialized lift-based foot and wing swimming (Fish 2016). Botton-Divet and collaborators analyzed morphological changes in the long bones of semi-aquatic mustelids (otters and minks) as compared to their terrestrial relatives and highlighted the joint effects of size, locomotor mode, and phylogeny on limb shape evolution and the difficulty to separate them (Botton-Divet et al. 2016). Blob and collaborators analyzed differences in the locomotor system between semi-aquatic and marine turtles. They illustrated the transformation of forelimb skeleton and associated musculature from tubular limbs with paddles used for rowing to flippers used for flapping. They also discussed the interactions between performance advantages and locomotor stability in this context (Blob et al. 2016). Lingham-Soliar and collaborators treated the convergences associated to the independent evolution of high-speed thunniform swimming in some ichthyosaurs and the lamnid shark Carcharodon. He presented the various associated adaptive features, including the fusiform body shape, crossed-fiber architecture of the skin, dorsal and caudal fins, caudal peduncle, and the ligamental series providing power transmission from anterior muscles through the peduncle to the caudal fin (Lingham-Soliar 2016). Pabst and collaborators presented the toolkit required to build a deep diver. Based on dissections and the weighing of different parts of the body (e.g., integument, muscles, organs, bones) as a percent of total body mass, they compared the deep-diving mesoplodonts (Cetacea) and elephant seal (Pinnipeda) to shallow-divers. They showed that deep-divers display similar integument and bone proportions, as compared to shallow divers, but relatively smaller brains and thoracic and abdominal viscera. Conversely they showed significantly larger locomotor muscles with a unique muscle fiber profile that suggests low rates of oxygen use. They suggested that these adaptive changes probably play a major role in reducing metabolic rate in these deep-diving taxa (Pabst et al. 2016).
Bone inner structure
Secondary adaptation to an aquatic life is associated with changes in inner organization of bone (= bone microanatomy; i.e., the distribution of the osseous tissue in bone) and in bone histology (i.e., collagen fiber orientation, cell distribution, vascularization). Houssaye and collaborators presented a review of the bone microanatomical specializations encountered in semi-aquatic and aquatic amniotes. Based on the analysis of vertebrae, ribs and stylopod long bones of numerous modern and fossil amniotes, they highlighted the important diversity of these patterns, as opposed to the two generally recognized types of osseous specializations (bone mass increase versus spongious organization). They also showed the important intraskeletal variation in the microanatomical features and the wide range of combinations observed. Based on these data, they discussed the link between microanatomical features and functional requirements in bones of secondarily aquatic amniotes (Houssaye et al. 2016). Canoville and de Buffrénil (2016) focused on microanatomical changes observed in the king penguin. They analyzed the ontogenetic and intraspecific variability in order to estimate limb bone microanatomical variability. They revealed important changes during ontogeny, which are linked to an intense remodeling episode during the juvenile molt. In addition, they observed that the various bones present distinct developmental patterns and that some variability occurs even in same bones of different adult specimens. Cooper and collaborators proposed to combine bone microanatomical and isotopic approaches on a large sample of modern and fossil cetartiodactyls to better reconstruct the origins of semi-aquatic habits in cetaceans. They found consistency between microanatomical and isotopic data and suggest that the common ancestor of anthracotheres, hippopotamids, raoellids, and cetaceans probably spent considerable time in water (Cooper et al. 2016).
The last study in this collection focused on bone histological features. Dumont and Houssaye examined marine squamates. They analyzed the vascular network in three dimensions of the vertebrae of stem-ophidiomorphs, marine snakes, and mosasaurs, in comparison to terrestrial modern squamates (Dumont and Houssaye, 2016). They showed clear differences in vascular organization and density (e.g., cortical vascularity, canal size diameter, orientation, degree of anastomoses) in accordance with physiological and locomotory changes in the progressive adaptation to an aquatic lifestyle, with clear differences pending on ecological grades.
These various contributions provide us a wider view of the numerous adaptive features associated with secondary aquatic lifestyle. These contributions should enable a consideration of all the adaptive features when focusing on a specific trait. Methodologies used for all these analyses were also very diverse. This symposium highlights the interest of combining data from different types of studies in order to better understand this major ecological shift, and shows the importance of including fossils in order to understand this key transformation at a large and long-term evolutionary scale.
We wish to thank the International Congress of Vertebrate Morphology for the opportunity to organize and present this symposium and its Program Officer, Lawrence Witmer, for his help and reactivity in facilitating and adjusting the organization of the symposium. And, of course, we warmly thank all participants to the Symposium and special issue for their great contributions.
There was no funding to support the symposium.