The Macroecology of Chemical Communication in Lizards: Do Climatic Factors Drive the Evolution of Signalling Glands?

Abstract

Chemical communication plays a pivotal role in shaping sexual and ecological interactions among animals. In lizards, fundamental mechanisms of sexual selection such as female mate choice have rarely been shown to be influenced by quantitative phenotypic traits (e.g., ornaments), while chemical signals have been found to potentially influence multiple forms of sexual and social interactions, including mate choice and territoriality. Chemical signals in lizards are secreted by glands primarily located on the edge of the cloacae (precloacal glands, PG) and thighs (femoral glands), and whose interspecific and interclade number ranges from 0 to > 100. However, elucidating the factors underlying the evolution of such remarkable variation remains an elusive endeavour. Competing hypotheses suggest a dominant role for phylogenetic conservatism (i.e., species within clades share similar numbers of glands) or for natural selection (i.e., their adaptive diversification results in deviating numbers of glands from ancestors). Using the prolific Liolaemus lizard radiation from South America (where PG vary from 0 to 14), we present one of the largest-scale tests of both hypotheses to date. Based on climatic and phylogenetic modelling, we show a clear role for both phylogenetic inertia and adaptation underlying gland variation: (i) solar radiation, net primary productivity, topographic heterogeneity and precipitation range have a significant effect on PG variation, (ii) humid and cold environments tend to concentrate species with a higher number of glands, (iii) there is a strong phylogenetic signal that tends to conserve the number of PG within clades. Collectively, our study confirms that the inertia of niche conservatism can be broken down by the need of species facing different selection regimes to adjust their glands to suit the demands of their specific environments.Electronic supplementary materialThe online version of this article (10.1007/s11692-018-9447-x) contains supplementary material, which is available to authorized users.

Unravelling associations among chemosensory system components in Liolaemus lizards

“…In Liolaemus lizards, the number of precloacal glands shows a strong phylogenetic pattern (Supporting Information Appendix and Fig. 3c; Pincheira‐Donoso, Hodgson & Tregenza, 2008; Jara et al ., 2018), as is the case in Squamata in general (García‐Roa et al ., 2017). However, in spite of this, there are different patterns in the phylogenetic signal of scents glands within each lizards group (García‐Roa et al ., 2017).…”

“…The number of scents glands may also respond to different selective forces associated with the experienced environmental conditions of species (e.g. altitude; Escobar, Labra & Niemeyer, 2001; substrate; Hews & Martins, 2013; Baeckens et al ., 2015; climate; Jara et al ., 2018) and therefore, its evolutionary pattern may also reflect responses to these conditions.…”

Investment in chemical signalling glands facilitates the evolution of sociality in lizards

“…These structures were probably absent in the lizard common ancestor, and repeatedly emerged and disappeared in squamate evolutionary history [35,42]. Because of their significance in chemical signalling, the absence of epidermal glands in lizards has been interpreted by some researchers as less reliance on chemical signals as an information source [35,[41][42][43][44][45]. A recent behavioural study showed that Liolaemus species with epidermal glands relied more upon chemical, rather than visual, signals for species recognition in contrast to species lacking glands, which appeared to rely predominantly on visual cues or signals for discriminating conspecifics and heterospecifics [77].…”

“…Liolaemus tenius females, for instance, are more attracted to substrates covered with male epidermal gland secretions than to substrates scent-marked with male skin extracts [40]. The occurrence (absence/ presence) of lizard epidermal glands is strictly species-specific and regularly used as a proxy of a species' investment and reliance upon chemical signalling [35,[41][42][43][44][45]. Lizards sample substrate-bound or airborne chemicals in the environment using tongue-flicking (vomerolfaction), or receive chemicalladen air through the nasal nares (olfaction s.s.) [46,47].…”

Hemipenes eversion behavior: a new form of communication in two Liolaemus lizards (Iguania: Liolaemidae)

“…In other lizard genera, it was proposed that the absence of pheromonal pores might be associated to an increased use of visual displays (e.g., Lacertidae and Phrynosomatidae; Hews and Benard 2001;Baeckens et al 2015). Based on the fact that lizards of the Chilean group have less precloacal pores than those of the Argentinean group (Laurent 1983;Jara et al 2018), Martins et al (2004) hypothesized that the former depended more on visual communication, while the latter might use the chemical modality more. Males of L. quilmes have an average of 5.8 precloacal pores (Etheridge 1993), but L. coeruleus males lack these pores completely (Cei and Ortiz-Zapata 1983).…”