Tempo and mode of performance evolution across multiple independent origins of adhesive toe pads in lizards

Abstract

Understanding macroevolutionary dynamics of trait evolution is an important endeavor in evolutionary biology. Ecological opportunity can liberate a trait as it diversifies through trait space, while genetic and selective constraints can limit diversification. While many studies have examined the dynamics of morphological traits, diverse morphological traits may yield the same or similar performance and as performance is often more proximately the target of selection, examining only morphology may give an incomplete understanding of evolutionary dynamics. Here, we ask whether convergent evolution of pad-bearing lizards has followed similar evolutionary dynamics, or whether independent origins are accompanied by unique constraints and selective pressures over macroevolutionary time. We hypothesized that geckos and anoles each have unique evolutionary tempos and modes. Using performance data from 59 species, we modified Brownian motion (BM) and Ornstein-Uhlenbeck (OU) models to account for repeated origins estimated using Bayesian ancestral state reconstructions. We discovered that adhesive performance in geckos evolved in a fashion consistent with Brownian motion with a trend, whereas anoles evolved in bounded performance space consistent with more constrained evolution (an Ornstein-Uhlenbeck model). Our results suggest that convergent phenotypes can have quite distinctive evolutionary patterns, likely as a result of idiosyncratic constraints or ecological opportunities.

The relationship between habitat use and body shape in geckos

“…A large body of work has shown that geckos exhibit sophisticated climbing behaviors and morphological specializations, such as toe‐peeling, a unique tendon structure, and other toepad modifications (e.g., blood‐filled sinuses and fat pads; Russell, ; Autumn et al, ). These behaviors and modifications result in gecko adhesive abilities that are more proficient than other toe pad‐bearing lizards of similar size (Hagey et al, ; Irschick et al, ). How these functional advantages are potentially translated into the use of a wider range of habitats remains an open question.…”

Nonlinear variation in clinging performance with surface roughness in geckos

“…Fields of microfibrillar setae adhere to contacted surfaces through van der Waals forces (Autumn, Dittmore, Santos, Spenko, & Cutkosky, ; Autumn et al, ; Tian et al, ). The ability to cling to substrates by means of subdigital pads has long been a topic of research (Collette, ; Delannoy, ; Elstrott & Irschick, ; Ernst & Ruibal, ; Gamble et al, ; Hagey, Puthoff, Holbrook, Harmon, & Autumn, ; Ruibal & Ernst, ), and several studies have aimed to determine factors that allow geckos to adhere to and detach from the substrates they move across, examining the locomotory substrate characteristics (Gillies et al, ; Meine, Kloss, Schneider, & Spaltmann, ; Persson & Gorb, ; Pugno & Lepore, ; Spolenak, Gorb, Gao, & Arzt, ), the mechanisms of adhesion (Autumn et al, ; Autumn, Niewiarowski, & Puthoff, ; Gao, Wang, Yao, Gorb, & Arzt, ; Irschick, Herrel, & Vanhooydonck, ; Mahendra, ; Tian et al, ), and variation in adhesion among species (Bergmann & Irschick, ; Garner, Stark, Thomas, & Niewiarowski, ; Hagey et al, , ; Irschick et al, ; Stark, Klittich, Sitti, Niewiarowski, & Dhinojwala, ; Stark et al, ).…”

“…The gekkotan adhesive system has evolved to enable the exploitation of inclined and inverted surfaces on rocks, or vegetation, with recent expansions onto man‐made structures by some species (Glossip & Losos, ; Gamble et al, ; Hagey et al, ; Ruibal & Ernst, ). The mechanism and dynamics of adhesion, however, have almost exclusively been examined using a variety of smooth (Autumn et al, ; Gillies & Fearing, ; Irschick et al, ; Peressadko & Gorb, ; Russell & Johnson, ; Stewart & Higham, ) and very fine‐grained man‐made surfaces (i.e., glass, Teflon, variations of polyethylene, polyvinyl chloride, aluminum bonding wire, acrylic, and acetate sheets; Campolo, Jones, & Fearing, ; Gillies & Fearing, ; Huber, Gorb, Hosoda, Spolenak, & Arzt, ; Meine et al, ; Persson, ; Persson & Gorb, ; Pugno & Lepore, ; Vanhooydonck, Andronescu, Herrel, & Irschick, ; Winchell, Reynolds, Prado‐Irwin, Puente‐Rolón, & Revell, ), most of them not encountered by geckos under natural conditions.…”

Systematics of the Saharo‐Arabian clade of the Palearctic naked‐toed geckos with the description of a new species ofTropiocolotesendemic to Oman

“…With more than 1,714 species in 124 genera inhabiting all warm continental land masses and thousands of intervening continental and oceanic islands, geckos are one of the most species‐rich, abundant, and widely distributed of all squamate lineages (Gamble et al., ; Pincheira‐Donoso, Bauer, Meiri, & Uetz, ; Uetz, Freed, & Hošek, ). Geckos are also very well known by the extraordinary climbing abilities of some of the groups, enabled by complex digital adhesive mechanisms whose evolution seems to be absent of substantial selective constraints, allowing them to adapt and interact with their environment in many different ways compared with other lizards (Gamble, Greenbaum, Jackman, Russell, & Bauer, ; Hagey et al., ). Another important trait of geckos is their ancestral nocturnal habits, still present in more than 70% of the species and with several independent transitions to diurnality and some secondary transitions back to nocturnality (Gamble, Greenbaum, Jackman, & Bauer, ).…”