Tetrapod-like pelvic girdle in a walking cavefish

Abstract

Fishes have adapted a number of different behaviors to move out of the water, but none have been described as being able to walk on land with a tetrapod-like gait. Here we show that the blind cavefish Cryptotora thamicola walks and climbs waterfalls with a salamander-like diagonal-couplets lateral sequence gait and has evolved a robust pelvic girdle that shares morphological features associated with terrestrial vertebrates. In all other fishes, the pelvic bones are suspended in a muscular sling or loosely attached to the pectoral girdle anteriorly. In contrast, the pelvic girdle of Cryptotora is a large, broad puboischiadic plate that is joined to the iliac process of a hypertrophied sacral rib; fusion of these bones in tetrapods creates an acetabulum. The vertebral column in the sacral area has large anterior and posterior zygapophyses, transverse processes, and broad neural spines, all of which are associated with terrestrial organisms. The diagonal-couplet lateral sequence gait was accomplished by rotation of the pectoral and pelvic girdles creating a standing wave of the axial body. These findings are significant because they represent the first example of behavioural and morphological adaptation in an extant fish that converges on the tetrapodal walking behaviour and morphology.

Musculoskeletal anatomy of the pelvic fin of Polypterus: implications for phylogenetic distribution and homology of pre‐ and postaxial pelvic appendicular muscles

“…For example, in the teleostean rainbow trout the pelvic fins are actively oscillated, damping body oscillation and altering flow direction downstream of the fins (Standen, 2010). The pelvic fin even performs tetrapod-like movements during locomotion in some fish, such as the lungfish Protopterus (King et al 2011) and the actinopterygian Cryptotora (Flammang et al 2016). A number of batoids (rays) and bottom-dwelling sharks such as Orectolobiforms use their pelvic fins in a walking or 'punting' motion against the substrate (e.g.…”

The structure and function of the sucker systems of hill stream loaches

“…It is also listed as vulnerable on the IUCN 98 red list (ICUN 2018). It is protected and is difficult to capture in the wild and therefore a challenging 99 animal to study (Flammang et al 2016). Here we contrast the Cryptotora thamicola skeletal structure 100 with the more accessible and captive bred Sewellia sp.…”

“…(These are illustrated with video sequences -see supplementary 91 material -locomotion). 92 The crawling mode of movement (type 1 above) has been the subject of recent scientific interest 93 because such movement is thought to be an evolutionary precursor to tetrapod walking on dry land 94 (Flammang et al 2016). In particular the skeletal structure of the walking cavefish (Cryptotora 95 thamicola) has been described; this species has developed a pelvic girdle and is able to climb 96 waterfalls in fast flowing water in caves and can walk up wet surfaces in air.…”

“…In particular the puboischiadic 288plate is the most prominent skeletal feature on both species(Fig 3). The pelvic girdle is similar to the 289 cave fish (Cryptotora thamicola)(Flammang et al 2016) in that one rib (called the pleural or sacral 290 rib) is hypertrophied and forms a closed loop with the puboischiadic plate. This pleural rib is 291 described bySawada (1982) as being connected to the puboischiadic plate by a strong ligament 292 (invisible in CT scan) in closely related species.293 CT scans of Gastromyzon punctilus (left) and Sewellia lineolata(right).…”

Amphibious fishes: evolution and phenotypic plasticity

“…Harris, 1960;Ellerby et al, 2001;Swanson and Gibb, 2004;Sayer, 2005;Gibb et al, 2011;Ashley-Ross et al, 2013;Pronko et al, 2013;Close et al, 2014;Pace and Gibb, 2014;Standen et al, 2014;Bressman et al, 2015;Flammang et al, 2016). One strategy is to rely on fixed adaptations that are a compromise for movement in air and water.…”