Document Type

Article

Language

eng

Publication Date

2020

Publisher

BioMed Central

Source Publication

BMC Ecology and Evolution

Source ISSN

1471-2148

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.

Background

Temporal niche, also known as diel activity niche, is an important aspect of the biology of an organism, necessitating the evolution of specialized morphology, physiology, ecology, and behavior (e.g. [19, 41, 56, 72]). For example, many diurnal ectotherms thermoregulate through basking behavior (i.e. heliothermy), whereas nocturnal ectotherms thermoregulate through contact with surfaces of different temperatures (i.e. thigmothermy; [1, 16, 51]). Temporal niche appears to be phylogenetically conserved across major tetrapod clades [2] and thus many adaptations to specific temporal niches (diurnal, nocturnal, crepuscular, or cathemeral) are shared among closely related species. Despite its conservation in tetrapod evolutionary history [2], several squamate clades do exhibit temporal niche turnover. The crown group of geckos (Infraorder Gekkota) are hypothesized to be ancestrally nocturnal, with reversals to diurnality occurring in at least 10 lineages [2, 24, 76]. Many of these lineages exhibit an array of diurnal-specialized adaptations, most notably eye morphologies, with oil droplets which aid in light filtering and spectral tuning [9, 55, 70, 76], concaviclivate temporal fovea to aid in binocular vision [57, 71], and ovoid retinal pigmented epithelia (RPE) to aid in light filtering and absorption [31, 65].

Comments

Published version. BMC Ecology and Evolution, Vol. 20, No. 40 (2020): 1-10. DOI. © 2020 BioMed Central. Used with permission.

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Creative Commons License

Creative Commons Attribution 4.0 License
This work is licensed under a Creative Commons Attribution 4.0 License.

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