Repeated evolution of digital adhesion in geckos: a reply to Harrington and Reeder

Abstract

We published a phylogenetic comparative analysis that found geckos had gained and lost adhesive toepads multiple times over their long evolutionary history (Gamble et al., PLoS One, 7, 2012, e39429). This was consistent with decades of morphological studies showing geckos had evolved adhesive toepads on multiple occasions and that the morphology of geckos with ancestrally padless digits can be distinguished from secondarily padless forms. Recently, Harrington & Reeder (J. Evol. Biol., 30, 2017, 313) reanalysed data from Gamble et al. (PLoS One, 7, 2012, e39429) and found little support for the multiple origins hypothesis. Here, we argue that Harrington and Reeder failed to take morphological evidence into account when devising ancestral state reconstruction models and that these biologically unrealistic models led to erroneous conclusions about the evolution of adhesive toepads in geckos.

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

“…Our reconstruction favored a single origin of toe pads within geckos, which is significantly fewer than previous work (Gamble et al 2012), although we cannot rule out multiple origins (see Gamble et al 2017). In order to incorporate historical information such as the repeated evolution of adhesive toe pads in lizards, we conducted an ancestral state reconstruction.…”

“…Gamble et al (2012) found toe pads to be associated with slightly higher rate of diversification, although this was not the case for Garcia-Porta and Ord (2013). Considering state-correlated diversification rate alongside an ancestral state reconstruction, Harrington and Reeder (2017) concluded a single origin of toe pads using a "hidden states" binary-state speciation and extinction model (Maddison et al 2007;Beaulieu et al 2013;Beaulieu and O'Meara 2016), although Gamble et al (2017) dispute these results due to potentially high Type 1 error rates (Davis et al 2013;Maddison and FitzJohn 2015;Rabosky and Goldberg 2015). Future studies may want to consider incorporating character-state correlated diversification information into ancestral state reconstructions using the recently published nonparametric FiSSE (Fast, intuitive, State-dependent, Speciation-Extinction) approach (Rabosky and Goldberg 2017;Zenil-Ferguson and Pennell 2017).…”

“…When considering other lines of evidence such as the variation in toe hyperextension anatomy within geckos (Russell 1979), it is likely that the true number of origins within geckos lies somewhere between one and many (Gamble et al 2017). Future studies investigating the origins of adhesive toe pads in lizards will benefit from considering multiple lines of evidence (Gamble et al 2017).…”

Evolution of pedal digit orientation and morphology in relation to acquisition and secondary loss of the adhesive system in geckos

“…According to Gamble et al (), the ancestral padstate for the following is considered equivocal: Ptenopus , Narudasia , and Nactus . Furthermore, a more recent ancestral state reconstruction analysis (Gamble et al, ) interprets the ancestral padstate for Homonota as equivocal, whereas Gamble et al, indicate Homonota to be secondarily padless. The more recent ancestral state reconstruction analysis (Gamble et al, ) also indicates that Narudasia festiva , Ptenopus , and SE Asian Cnemaspis are secondarily padless.…”

“…The gecko adhesive system, which facilitates locomotion on smooth surfaces (Autumn 2000), is purported to have originated at least 11 times (Gamble, Greenbaum, Jackman, Russell, & Bauer, , ), with at least one origin in four of the six gecko families. Previous studies have suggested how gecko foot morphology is expected to change with the acquisition of an adhesive system (Russell, , ; Russell, Bauer, & Laroiya, ).…”