The concept that an animal’s form has evolved in response to the way it navigates its habitat underpins the study of ecomorphology—the intersection of organismal morphology, life history, and adaptation (Van der Klaauw 1948; Wainwright and Reilly 1994). Many studies have shown that locomotor performance is linked to morphology and strongly associated with structural features of the environment (i.e. ecomorphological specialization; Losos 1990, 2009, Luxbacher and Knouft 2009, Kaliontzopoulou et al. 2010a). Within diurnal lizards, ecomorphology has been well-studied in a number of ecologically diverse lineages of skinks, anoles, tropidurines, and wall lizards (Melville and Swain 2000; Bergmann and Irschick 2010; Kaliontzopoulou et al. 2010a; Losos 2010; Lee et al. 2013; Pincheira-Donoso and Meiri 2013; Pincheira-Donoso et al. 2015; Grismer et al. 2018; Toyama 2017) but comparatively little has been done on nocturnal lizards—and most of those involved only a single gekkonid genus (Grismer et al. 2015; 2017; 2020; Grismer and Grismer 2017; Nielson and Oliver 2017; Nguyen et al. 2021; Kaatz et al. 2021).

The Night Lizard family Xantusiidae is a New World lineage composed of three genera and 35 generally nocturnal species that collectively range from Southwestern North America to southern Central America (Noonan et al. 2013; Uetz et al. 2021). The family is dominated by highly cryptic, reclusive species with low vagility (Zweifel and Lowe 1966; Fellers and Drost, 1991; Mautz 1993) where high degrees of microhabitat specialization drive their differing ecomorphologies (Bezy 1989a, 1989b; Noonan et al. 2013). Within southern California, the Xantusiidae is represented by four, possibly five species of Xantusia bearing three trenchantly different ecomorphs and four different microhabitat preferences (Fig. 1): X. riversiana, an insular habitat generalist (Mautz 1993; Fellers and Drost 1991; Fellers et al. 1998); species of the X. vigilis complex (sec. Leavitt et al. 2007), vegetative specialists (Zweifel and Lowe, 1966); and X. gracilis and X. hensahwi, “rock-crevice-dwelling” (sec. Leavitt et al. 2007) specialists (Grismer and Galvin 1986; Lee 1975, respectively). Nonetheless, there have been only limited discussions extolling the ecomorphological differences between rock-crevice species and vegetation specialists within the genera Lepidophyma and Xantusia (Bezy 1967; Ramírez-Bautista et al. 2008; Adams et al. 2018) and only limited data have been generated to quantitatively evince the degree of morphological differences between the rock-crevice species X. henshawi—a granite exfoliation specialists (Lee 1975) and X. gracilis—a more generalized sandstone inhabitant (Grismer and Galvin 1986). Using a limited number of metrics, Grismer and Galvan (1986) noted differences in head proportions and the growth trajectories of body width and limb length, suggesting these were correlated with the more “terrestrial” life-style of X. gracilis. In the analyses herein, multivariate and univariate tests are used to quantify morphometric differences between X. gracilis and X. henshawi using an expanded data set comprised of 22 characters that have proven useful as ecomorphological indicators across a wide taxonomic range of lizard groups (Losos 1990, 2009, 2010; Melville and Swain 2000; Luxbacher and Knouft 2009, Bergmann and Irschick 2010; Kaliontzopoulou et al. 2010a; Lee et al. 2013; Pincheira-Donoso and Meiri 2013; Pincheira-Donoso et al. 2015; Grismer et al. 2015, 2018, 2020; Grismer and Grismer 2017; Nielson and Oliver 2017; Toyama 2017; Kaatz et al. 2021). These data are compared to similar data generated from distantly related lizard groups as leverage to generate preliminary hypotheses as to the adaptive significance of how the different ecomorphologies between X. gracilis and X. henshawi may correlate with their structurally different microhabitats.

The PCA demonstrates that Xantusia gracilis and X. hensahwi occupy non-overlapping positions in morphospace among the collective ordination of the first two principal components (Fig. 3A). Principal component 1 accounts for 24.3% of the variation and loads most heavily for limb width (FLW and HLW), thigh length (HL1), head width (HW) and snout width (SW) (Fig. 3C; Table 2). Principal component 2 accounts for an additional 15.3% of the variation and loads most heavily for head depth (HD), brachial length (FL1), fourth finger length (FL4), axilla-groin length (AG), pelvic height (PH), tibia length (HL2) and fourth toe length (HL4). Principal components 3 and 4 account for an additional 10.0% and 8.4%, of the variation, respectively (Fig. 3C; Table 2). Retention of the first seven eigenvalues of the DAPC, accounting for 93.3% of the variation, further recovered complete separation of X. gracilis and X. henshawi along the first discriminant function (Fig. 3B).

Although Xantusia gracilis and X. henshawi do not differ significantly in SVL, they do differ in a number of other proportions. The Student’s and Welch’s t-tests of the adjusted data recovered 11 characters bearing statistically significant mean differences between them (Fig. 4; Table 3), illustrating that X. gracilis has a significantly wider head (HW), longer snout (SL), larger eyes (ED), wider sternum (SW), thinner limbs (FLW and HLW, i.e. reduced limb mass), longer forearms (FL2), longer thighs (HL1), and a wider and higher pelvis (PW and PH, respectively). Welch’s t-test also demonstrated that X. gracilis has significantly longer hind limbs (HLL) than X. henshawi but not significantly longer forelimbs (FLL). Grismer and Galvin (1986) also noted that X. gracilis had a thinner body (inter-forelimb and inter-hind limb distances) than X. henshawi. Although X. gracilis has a longer snout, it does not have a significantly longer head and similarly, it has a significantly longer forearm, but does not have a significantly longer foreleg. These metrics indicate that not all components of the head and forelimb scale isometrically (i.e. they do not grow at the same rate).

The quantification of ecomorphological differences among species is important to many downstream analyses based on body size and shape. These types of data are not just necessary for comparative methods that combine phylogenies with phenotypic data to understand evolutionary processes such as the mode and tempo of trait evolution (Mahler et al. 2010). They also apply to a multitude of ecological principles where phenotypic differences within and among populations can influence the rate and direction of evolution, population dynamics, and the outcome of several other community interactions (Bolker et al. 2003; Werner and Peacor 2003; Krohne 2018).

These data clearly demonstrate that Xantusia gracilis and X. henshawi are proportioned differently and do not scale equally across various components of their bodies. Overall, X. gracilis is more slender and less robust than X. henshawi (Fig. 5) as was first reported by Grismer and Galvin (1986) using a limited data set. They inaccurately suggested these differences correlated with a more “terrestrial” life style. Using an expanded, more highly partitioned data set, however, reveals precisely where such differences occur and aptly justifies functional ecomorphological comparisons and inferences across a wide range of distantly related lizard groups bearing the same traits. It is logical to posit that the morphological differences between X. gracilis and X. henshawi are somehow related to their abilities to navigate their respective microhabitats. It has been well-established in a number of small clades of very closely related lizard species, that longer and thinner limb components increase climbing performance and are ecomorphological adaptations for a scansorial life style, as opposed to shorter, more robust limbs that occur in their less scansorial or strictly terrestrial (non-climbing) close relatives (Grismer and Grismer 2017; Neilson and Oliver 2017; Grismer et al. 2021; Kaatz et al. 2021). We hypothesize here, that these same adaptations in X. gracilis help it to navigate a more complex heterogeneous and less firm, topographically complex sandstone substrate (i.e. sandstone is not necessarily a flat, smooth, hardened surface; Fig. 2C) as compared to a more homogeneous, relatively flat, hardened granite boulder substrate (Fig. 2D). The smaller eye diameter (and obligatorily flatter head) and shorter pelvic height of X. henshawi would be more adaptive for taking refuge within narrow, restrictive retreats beneath granitic exfoliations and cap rocks (Fig. 2D). Although both species share adaptions for a scansorial, saxicolus life style—trenchantly different from that of strictly terrestrial species (e.g. X. riversiana)—differences in the complexity of their associated microhabitats are likely the driver of their ecomorphologicial differences.

What little work has been done looking at morphological adaptations related to climbing and clinging ability among closely related species living on different rock substrates is illustrative. In the eublepharid gecko genus Goniurosaurus, Grismer et al. (2021) demonstrated that the highly scansorial G. catbaensis, G. huuliensis, and G. luii, which are adapted to topographically complex karstic substrates, have significantly longer limbs, wider heads, longer snouts, and larger eyes than does the less scansorial G. lichtenfelderi that is adapted to a less complex granite substrate. Similarly, Cobos et al. (submitted), has shown experimentally, that reduced limb mass (i.e. thinner limbs), longer limbs, smaller hands and feet, and shorter digits, underpin the superior clinging ability of karst-adapted gekkonid species in the Cyrtodactylus pulchellus group as opposed to their closely related granite-adapted species. The point is, that very closely related saxicolus species navigating different rocky substrates are proportioned differently and that there may be a general convergence in relative limb and head proportions shared among those species that lead a more scansorial life style on topographically complex substrates.

The above research opens up several avenues of inquiry as to the locomotor performance between Xantusia gracilis and X. henshawi on their respective substrates as compared to that on one another’s substrate. Experimental trials such as those done by Cobos et al. (submitted) where climbing and clinging ability are measured on different substrates among different ecomorphs, could be used to test the morphology-based inference here that a complex sandstone habitat and a more homogenous granitic substrate require different ecomorphologies. Additionally, similar experiments can be designed to test the effects of unequal scaling in the various components (e.g. different limb and head dimensions) within functional systems (e.g. the limbs and skull) in order to ascertain what adaptive value different allometric trajectories may have during the course of ontogeny. Kaliontzopoulou et al. (2010a, 2010b) have shown that plasticity in limb trait variation in the saxicolus Podacris bocagei (Lacertidae) is under the influence of total body size. Whereas habitat-related differentiation is amplified for other limb characters when size effects are removed, and for others, it is completely eliminated or even reversed. Studying the ontogeny of limb traits in X. gracilis and X. henshawi (Grismer in prep.) may help to understand the putatively adaptive mechanisms underlying their ecomorphological differences.