The evolution of tail length in snakes associated with different gravitational environments

Abstract

Summary Gravity imposes potentially important constraints on blood circulation in tall or elongate animals during upright posture or climbing. Upright postures create vertical gradients of gravitational (=hydrostatic) pressures within circulatory vessels. In terrestrial animals, this pressure potentially induces blood pooling and oedema in dependent (inferior) tissues and, secondarily, decreases blood volume reaching the head and vital organs. Arboreal snakes exhibit a suite of adaptations for countering the effects of gravity on blood circulation, including relatively non‐compliant tissue compartments in the tail. However, patterns of tail length related to arboreal habitats and gravity have not been previously studied. Here, we test the hypothesis that arboreal snakes have relatively longer tails than non‐climbing species, and we interpret the results within the context of adaptation to gravity stress. Length data were obtained for 226 snake species, 139 genera and 15 snake families assigned to three broad gravitational habitat categories (G‐habitats: stenotopically arboreal, eurytopically arboreal/terrestrial and non‐scansorial). We constructed a composite phylogenetic tree and quantified the relationships between snake morphology and G‐habitat using conventional regression analysis of species data and regressions of phylogenetically independent contrasts. Mean relative tail length (RTL) increased and mean relative snout‐vent length decreased with increasing arboreality among the three G‐habitats. However, mean total body length (TL) was not different between the two arboreal G‐habitats. Snakes with longer RTLs have a higher percentage of elongate blood vessels contained within the relatively non‐compliant integument of the tail, which mitigates postural blood pooling experienced during climbing. TL in adult female arboreal snakes is hypothesized to be an evolutionary trade‐off between demands for a longer tail to enhance cardiovascular performance and the length of body cavity to provide space for young. Our results complement previous studies correlating RTL with arboreal habitat use, in addition to physiological experiments quantifying the effects of gravity on blood flow in snakes. These results provide evidence that long RTLs of arboreal snakes function, at least in part, as an adaptive response to cardiovascular stresses on blood circulation imposed by gravity. Selection on tail length related to other factors seems less likely, but is in need of further investigation.

Small mammals have big tails in the tropics

“…Meanwhile, arboreal and scansorial snakes are known to have long tails (Sheehy, Albert, & Lillywhite, ), and snake tail length varies systematically with climate in a way that is consistent with this generalization (Lawing, Head, & Polly, ). The underlying reason is thought to be physiological and unrelated to locomotion, but it remains possible that the snake pattern relates to grasping performance (Sheehy et al, ).…”

Ecological specialization and morphological diversification in Greater Antillean boas

“…; Feldman and Meiri ), such that arboreal specialist snakes tend to be slender and lightweight, with longer prehensile tails and different axial skeletal musculature (Jayne ; Lillywhite and Henderson ; Sheehy et al. and references therein). In Chilabothrus , arboreal specialists are not only smaller bodied than substrate generalists, they tend to have elongate and slender bodies.…”

“…Small species are generally characterized by a completely saurophagus diet and specialized adaptations to terrestrial (C. exsul and C. fordii) or arboreal (C. gracilis, C. monensis, and C. granti) substrates. Substrate specialization, such as arboreality, influences body proportions (Lillywhite and Henderson 1993;Pizzatto et al 2007b;Feldman and Meiri 2013), such that arboreal specialist snakes tend to be slender and lightweight, with longer prehensile tails and different axial skeletal musculature (Jayne 1982;Lillywhite and Henderson 1993;Sheehy et al 2016 and references therein). In Chilabothrus, arboreal specialists are not only smaller bodied than substrate generalists, they tend to have elongate and slender bodies.…”

Arboreality constrains morphological evolution but not species diversification in vipers

“…Of particular interest is arboreality, which emerged multiple times during the evolutionary history of snakes [21]. Arboreal snakes are known to possess a suite of behavioural, morphological and physiological adaptations that allow elongated and limbless organisms to address the challenges of living in a structurally complex environment [21][22][23]. For example, heavier snakes would not be able to properly move among trees due to the fragility of tree branches, and snakes with shorter tails would lack the ability to hold branches, which would cause suboptimal locomotion in arboreal microhabitats [21 -23].…”