Distinct patterns of pigment development underlie convergent hyperpigmentation between nocturnal and diurnal geckos (Squamata: Gekkota)

Abstract

Background: Evolutionary transitions in temporal niche necessitates specialized morphology, physiology, and behaviors. Diurnal, heliothermic squamates (lizards and snakes) that bask require protection from ultraviolet radiation (UV) that can damage internal organs such as the brain, viscera, and gonads. Many smaller squamates have accomplished this protection by hyperpigmentation of the peritoneum and subcutaneous dorsum. Typically, nocturnal species do not require these protections from ultraviolet light. However, some nocturnal species that exhibit extreme crypsis may be exposed to sunlight and UV and require some means of mediating that damage. One such species is Gekko (Ptychozoon) kuhli, a nocturnal, arboreal gecko that uses extreme crypsis to blend in with tree bark. Hiding motionless on tree trunks leaves geckos exposed to sunlight during the day. Thus, we predict that G. kuhli will have independently evolved a hyperpigmented phenotype. To investigate this hypothesized association between temporal niche, behavior, and morphology, we characterized adult subcutaneous pigment for eight gecko species and embryonic pigment accumulation for a subset of four of these species, exhibiting diverse temporal niche and thermoregulatory behaviors. We predicted that nocturnal/potentially-heliothermic G. kuhli would exhibit hyperpigmentation of internal structures like that of diurnal/heliothermic geckos. We further predicted that embryonic pigment accumulation of G. kuhli would resemble that of diurnal/heliothermic as opposed to nocturnal/ thigmothermic geckos. Results: We found that temporal niche and thermoregulatory behavior predicted the degree of subcutaneous pigment in the eight gecko species examined. We demonstrate that G. kuhli accumulates pigment extremely early in embryonic development, unlike a diurnal/heliothermic gecko species, despite having a similar adult phenotype. Conclusions: The evolution of hyperpigmentation in G. kuhli is likely an adaptation to limit damage from occasional daytime UV exposure caused by crypsis-associated basking behavior. Gekko kuhli achieves its hyperpigmented phenotype through a derived developmental pattern, not seen in any other lizard species investigated to date, suggesting novel temporal differences in the migration and/or differentiation of reptilian neural crest derivatives.

At the edge of extinction: a first herpetological assessment of the proposed Serra do Pingano Rainforest National Park in Uíge Province, northern Angola

“…The difference in pigmentation was stable even under different, day/night light conditions and is still observable in ethanol-preserved material. The environmental drivers of this colour dimorphism deserve further study (see Griffing et al 2020).…”

Ocular elongation and retraction in foveated reptiles

“…Examples of this phenomenon can be seen in Figures 2 and 3 of the publication by Guerra-Fuentes and colleagues addressing the embryology of the retinal pigmented epithelium in five species of sphaerodactyls, 38 and in Figures 3 and 4 of the publication by Griffing, Gamble and Bauer addressing pigment development in nocturnal gekkonids (Gekko kuhli, Lepidodactylus lugubris) and diurnal gekkonids (Phelsuma laticauda, Sphaerodactylus macrolepis). 39 Among mammals, asymmetric globe development has been observed only for foveated haplorrhine primates but not for non-foveated primates or other mammalian species. [30][31][32][33][34][35][36][37] Together, these observations suggest that fovea morphogenesis is similar among foveated vertebrates.…”

“…We pay particular attention to alterations in ocular globe shape, which is an interesting, but poorly understood, aspect of eye development. Although typically only studied postnatally in the context of myopia in humans, [27][28][29] changes in ocular shape during embryonic development have been observed in a number of foveated species, including humans, [30][31][32][33][34][35][36] and non-human primates, 32,37 as well as geckos, 38,39 suggesting the presence of a conserved morphogenetic mechanism. The bifoveated brown anole is a good model system in which to study the mechanisms underlying fovea development in a vertebrate eye.…”

Ocular elongation and retraction in foveated reptiles

“…Examples of this phenomenon can be seen in Figures 2 and 3 of the publication by Guerra-Fuentes and colleagues addressing the embryology of the retinal pigmented epithelium in five species of sphaerodactyls, 32 and in Figures 3 and 4 of the publication by Griffing, Gamble and Bauer addressing pigment development in nocturnal gekkonids ( Gekko kuhli, Lepidodactylus lugubris ) and diurnal gekkonids ( Phelsuma laticauda, Sphaerodactylus macrolepis ). 33 Among mammals, asymmetric globe development has been observed only for foveated haplorrhine primates but not for non-foveated primates or other mammalian species. 24-31 Together, these observations suggest that fovea morphogenesis is similar among foveated vertebrates.…”

“…We pay particular attention to alterations in ocular globe shape, which is an interesting, but poorly understood, aspect of eye development. Although typically only studied postnatally in the context of myopia in humans, 21-23 changes in ocular shape during embryonic development have been observed in a number of foveated species, including humans, 24-30 and non-human primates, 26,31 as well as geckos, 32,33 suggesting the presence of a conserved morphogenetic mechanism. The bifoveated brown anole is a good model system in which to study the mechanisms underlying fovea development in a vertebrate eye.…”