At What Cost? Trade-Offs and Influences on Energetic Investment in Tail Regeneration in Lizards Following Autotomy

Abstract

Caudal autotomy, the ability to shed a portion of the tail, is a widespread defence strategy among lizards. Following caudal autotomy, and during regeneration, lizards face both short- and long-term costs associated with the physical loss of the tail and the energy required for regeneration. As such, the speed at which the individual regenerates its tail (regeneration rate) should reflect the fitness priorities of the individual. However, multiple factors influence the regeneration rate in lizards, making inter-specific comparisons difficult and hindering broader scale investigations. We review regeneration rates for lizards and tuatara from the published literature, discuss how species’ fitness priorities and regeneration rates are influenced by specific, life history and environmental factors, and provide recommendations for future research. Regeneration rates varied extensively (0–4.3 mm/day) across the 56 species from 14 family groups. Species-specific factors, influencing regeneration rates, varied based on the type of fracture plane, age, sex, reproductive season, and longevity. Environmental factors including temperature, photoperiod, nutrition, and stress also affected regeneration rates, as did the method of autotomy induction, and the position of the tail also influenced regeneration rates for lizards. Additionally, regeneration could alter an individual’s behaviour, growth, and reproductive output, but this varied depending on the species.

Ontogeny and caudal autotomy fracture planes in a large scincid lizard, Egernia kingii

“…Our results show that, for E. kingii , caudal autotomy fracture planes are not lost or restricted to a portion of the tail ontogenetically, with all specimens assessed from the ontogenetic growth series possessing intra-vertebral fracture planes throughout their post-pygal vertebrae. Although juvenile E. kingii rely heavily on caudal autotomy 24 , the complete retention of fracture planes and the ability to autotomise their tails as adults likely indicate that a net benefit from autotomy still applies to mature individuals 1 , 12 , 14 , 18 .…”

“…Adults are likely to live upwards of 15–20 years, similar to the related E. cunninghami 33 , giving them a longer reproductive span compared to short-lived, fast-maturing species. Ontogenetic retention of caudal autotomy planes may allow E. kingii to balance the reproductive costs of caudal autotomy as adults through their longevity and future reproductive seasons, with retention of this nascent strategy serving as a last resort scenario and conveying an overall fitness benefit to the species 12 .…”

“…Once autotomised, the tail regenerates over time, with the original bony vertebrae replaced by a rigid cartilaginous rod that lacks autotomy planes 6 , 7 . Although caudal autotomy is a very effective anti-predation strategy, how much of the tail is autotomised and the time and energy invested into regenerating the tail, can incur short- and long-term costs associated with locomotion, growth, reproduction and subsequent survival 8 – 12 . The fitness costs however, both short- and long-term, can potentially be mitigated in certain species depending on specific life-history characteristics and behavioural traits 12 .…”

The regenerating tail of lizard transits through a tumour‐like stage represented by the regenerative blastema

“…Therefore while some mesenchymal cells and fibroblasts are located distally underneath the apical wound epidermis, the proximal cells of the forming blastema are in contact with stump tissues (Figure 1c). The latter are represented by muscles, vertebral bone, nerves, spinal cord, adipose cells and other connective cells in case the tail was amputated by cutting or tearing, or mainly by connective fibroblasts of the autotomous connective septa in case of natural release of the tail by autotomy (Barr et al, 2021). In both cases, traumatic events (predators, fighting with conspecifics or from experimental intervention) or by induced voluntary release (autotomy), the tail regenerates.…”