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

Abstract

AbstractHuman influence has historically exerted a major driving in creating novel ecological niches. Although the controlled use of fire by ancient humans probably played a significant role by attracting positive phototactic prey and favour foraging by insectivorous vertebrates, no study has ever explored this possibility. Using a multidisciplinary approach, we explore whether human-controlled fire has historically affected the temporal niche partitioning in two lineages of Moorish geckosTarentola mauritanica, a diurnal- dark form and a nocturnal-pale form. We showed that the nocturnal-pale variant possesses lower skin melanin for fewer and smaller melanosomes and experiences lower α-MSH plasmatic levels than its diurnal-dark counterpart. Additionally, the analysis of the full mitochondrial genome established that our pale-nocturnal lineage emerged around 40,000 years ago, i.e., 20,000 years before the dark-diurnal lineage. Both variants arose when modern humans expanded into Europe, coinciding with the widespread use of fire, which likely facilitated the availability of arthropod prey for pale geckos, opening a previously untapped niche. Our modelling exercises corroborated a highly probable human-geckos coexistence during the emergence of these lineages. Furthermore, we experimentally demonstrated that fire near a rock surface significantly increases the abundance of arthropod prey, attracting preferred prey for the pale variant during nocturnal foraging. We suggest that ancient fires likely provided a novel foraging niche for pale geckos, yet it remains unclear whether the two lineages originated from diurnal or nocturnal ancestors. We present two alternative interpretations: the “out of the dark” scenario proposes a nocturnal ancestor leading to a diurnal descendant, while the “into the dark” scenario suggests a dark-diurnal ancestor evolving into a pale-nocturnal lineage. Phenotypic plasticity emerges as a critical factor in both scenarios, facilitating adaptation to new environments. We underscore the ongoing impact of artificial lighting on nocturnal behaviour, offering parallels to the potential origins of the gecko’s nocturnal lineage.