Flame-forged divergence? Ancient human fires and the evolution of diurnal and nocturnal lineages in moorish geckos

Abstract

Using a multidisciplinary approach, we investigated whether human-controlled fire has historically influenced temporal niche partitioning between dark-diurnal and pale-nocturnal lineages of the Moorish gecko (Tarentola mauritanica). The pale-nocturnal variant exhibited lower skin melanin levels, smaller and fewer melanosomes, and lower plasma α-Melanocyte Stimulating Hormone levels than its dark-diurnal counterpart. Mitochondrial genome analyses indicated that the common ancestor of these gecko lineages diverged approximately 6,600 years ago, coinciding with the transition of modern humans from nomadic hunter-gatherers to settled agricultural societies. Species distribution models suggested coexistence between humans and geckos during the emergence of these lineages. Additionally, we demonstrated that fire attracts phototactic arthropods, concentrating prey resources. These findings imply that human-controlled fire may have created a novel foraging niche for pale-nocturnal geckos, likely driving the divergence of the two variants.

Keywords: Evolutionary biology; Phylogenetics; Zoology.

Graphical abstract

Figure 1

Dark-diurnal (A) and pale-nocturnal (B) Moorish geckos (Tarentola mauritanica) morphotypes The two lineages occupy distinct ecological niches: the diurnal form inhabits trees, while the nocturnal variant prefers building walls at night. Insets (C) and (D) show the plasticity of a dark-diurnal gecko changing skin color on different substrates (see for more details). The bar scale is representative of 1mm (see also Figure S1).

Figure 2

Comparisons between the two geckos’ morphotypes Comparisons between dark-diurnal (“day”) and pale-nocturnal (“night”) Moorish geckos (Tarentola mauritanica) for (A) Integral under skin reflectance curve, (B) spectrophotometric skin melanin assay (ng/μg protein) and C) α-MSH hormone blood concentration (mg/mL). Data are presented as boxplots showing the mean (dotted line), median (bold line), interquartile range (box), and whiskers representing ±1 standard deviation. Individual data points are shown as dots. One-way ANOVA tests, ∗∗p < 0.001 (see also Tables S1–S3).

Figure 3

Skin sections stained with toluidine blue (A) Skin from the dorsal area of dark-diurnal Moorish geckos (Tarentola mauritanica), with single melanophores (inset). A high concentration of melanophores (thick arrow) is localized in the dermal region, along with a thick layer of melanin granules (arrow). (B) Digitally stained version of image A to emphasize melanophores and melanin pigment. (C) Skin from the dorsal area of a pale-nocturnal gecko, with a single melanophore (inset). (D) Digitally stained version of image C to emphasize melanophores and a layer of melanin pigment. The bar scale is representative of 50μm.

Figure 4

Past sympatry between Tarentola mauritanica and Homo sapiens (A, B, and C) Spatial distribution models of T. mauritanica and H. sapiens and their overlap during the time interval 0.06 Myr−0.02 Myr. The models indicate significant overlap in potential distribution within the Mediterranean region, supported by a linear mixed-effect model demonstrating a positive relationship between potential distributions of the two species. (D) Spatial distribution model of T. mauritanica approximately 10,000 years ago (Boyce Index, Spearman correlation test and the linear mixed-effects model p < 0.001). (E) Distribution of the 317 ancient genomes of H. sapiens mainly from the Mesolithic and Neolithic periods (filled squares, modified from⁴¹) and further archaeological records (see also Figure S2; Table S4). The bar scale is representative of 500 km of distance.

Figure 5

Phylogenetic characterization (A) Phylogeny and divergence time estimation derived from molecular-clock analysis of 10 pale-nocturnal (N1-N10) and 6 dark-diurnal (D1-D6) Tarentola mauritanica, in addition to other Italian haplotypes. Divergence times for the two gecko populations were calculated using the complete mitochondrial genome. The red bars on the nodes represent the 95% credibility intervals of the estimated posterior distributions of the divergence times. The bar scale is representative of 1 Kya, thousand years ago. (B) DensiTree. All trees created in the analysis (except the burn-in phase) are displayed. Trees with the most common topology are highlighted in dark green, and trees with the second most common topology in light green.

Figure 6

Characterization of trophic availability Numbers of arthropods collected from walls exposed to fire (F) vs. walls not exposed to fire (NF). (A) Sankey diagram connecting numbers of individuals collected by order with treatment. (B) The total number of individuals captured under the two conditions is shown. Data are represented as boxplots with the mean (dotted line), median (bold line), interquartile range (box), and whiskers representing ±1 standard deviation. (two-tailed t-test; t = 2.50; d.f. = 9; p < 0.05) (see also Table S5).