Evolution and diversification of the geckos of the Arabian Peninsula and Socotra Archipelago, compared to other mainland-island systems

Abstract

A major challenge in evolutionary biology is understanding the main drivers that underlie morphological and species diversity. Ecological opportunity—access to new or previously inaccessible niches—has been identified as one of the most important drivers of both phenotypic and species diversification. This is because the exploitation of new ecological niches is often accompanied by phenotypic differentiation among closely related taxa. This can in turn facilitate species diversification if phenotypic differentiation is associated with the appearance of reproductive isolation. The main goal of this thesis is to explore the extent in which a major source of ecological opportunity—the colonization of islands—have driven evolutionary diversification in different taxonomic and geographic contexts, specifically in the geckos of Arabia and the Socotra Archipelago and the Australasian diplodactyloid geckos. Island colonization is thought to provide a context of many available resources with few competitors and predators. This allows to colonizing groups the possibility to experience an “ecological release” and use a wider array of niches compared to their continental close-relatives. In such a situation, we expect an expansion of the morphospace in island groups typically associated with high rates of phenotypic and species diversification. We have found compelling evidence for this in both of the two mainland-island systems studied. The Australasian diplodactyloid geckos clearly expanded the range of phenotypic variation existing in the continent, producing the biggest and the smallest species in the radiation and were associated to accelerated rates of body size diversification compared to their closest relatives in the continent. Likewise, in the Hemidactylus geckos from Arabia-Socotra, island species were also associated to accelerated rates of phenotypic diversification and, as in the Australasian system, produced the most extreme sizes in the radiation. In this last mainland-island system, aside of reaching the maximum and the minimum sizes, the body size disparities in continental species assemblages were always significantly greater than the disparities computed by continental species assemblages. Nonetheless, when we compare Hemidactylus to other groups diversifying in the same islands, it appears that not all groups equally tend to diversify in body size. In fact, the comparison of the stages of diversification between the three gecko genera occurring in the Archipelago of Socotra revealed that not a single path of intra-island diversification was shared by all genera. Hemidactylus and Haemodracon greatly diversified in body size. However, in Pristurus diversification was strongly mediated by climatic shifts with size diversification being displaced to a subtle role. This is an important result as suggests that not all groups respond in the same way to similar amounts of ecological opportunity and that group-dependent (intrinsic) components can potentially play a role at defining the different stages of diversification. Aside of these examples of island diversification, in this thesis I also exposed remarkable examples of “island-like” patterns of diversification occurring in the continent. This was the case for the Australasian Pygopodidae, which attained rates of phenotypic diversification (possibly species diversification too) comparable to those found in island groups and was mostly mediated by the acquisition of a remarkable key innovation: a “snake-like” phenotype. Another remarkable example of continental diversification revealed in this thesis is a complex of highly divergent species existing within the subspecies Pristurus rupestris rupestris. This diversification took place in truly “island-like” setting, the Hajar Mountains in southeastern Arabia, formed by three main isolated blocks or “sky islands”. However, in this case diversification failed to take place within each of the “islands” and mostly was driven through intermittent pulses of dispersal and isolation taking place between two of the two main mountain blocks. Examples like this provide an example of how continental groups in some contexts, as the ones offered by mountain ranges, can fuel substantial amounts of diversification. In this case one of the greatest vertebrate diversification in Arabia.

Uno de los retos más importantes en biología evolutiva es entender las causas principales de la diversidad de fenotipos y de especies. La oportunidad ecológica (o el acceso a recursos nuevos y previamente inaccesibles) se considera como uno de los factores más importantes en la generación de nuevas especies y fenotipos. El objetivo principal de esta tesis es estudiar el papel generador de especies y fenotipos de uno de los grandes tipos de oportunidad ecológica, la colonización de islas. Para ello, se han usado dos sistemas continente-isla como modelo: los gecos de Arabia y el Archipiélago de Socotra y los gecos diplodactiloideos australasiáticos. Dado que las islas proporcionan ambientes con pocos competidores y depredadores, esto permite a los grupos insulares experimentar una gran expansión de nicho que puede estar asociada a una expansión del morfoespacio mediada por tasas elevadas de diversificación fenotípica y de especies. Los resultados de esta tesis respaldan totalmente esta hipótesis. Tanto en los gecos australasiáticos como en los gecos de Arabia y Socotra, la colonización de islas vino acompañada con aumentos sustanciales de disparidad fenotípica asociados con incrementos en las tasas de diversificación de tamaños del cuerpo y de especies. Aunque esto subraya la gran capacidad que tienen los entornos insulares en promover diversificación, diferentes grupos diversificando en las mismas islas no necesariamente siguen caminos evolutivos equivalentes. En el archipiélago de Socotra, la diversificación intra-isla en los géneros Hemidactylus y Haemodracon estuvo acompañada de grandes cambios del tamaño del cuerpo, que sólo posteriormente derivaron en cambios macroecológicos. Por el contrario, en el género Pristurus, la diversificación intra-isla fue principalmente mediada por cambios macroecológicos, siendo la diversificación del tamaño del cuerpo casi inapreciable. Esto demuestra que grupos cercanos diversificando en las mismas islas, pueden presentar patrones de diversificación completamente dispares. Al margen de las diversificaciones intra-isla expuestas, los resultados de esta tesis también han expuesto importantes patrones de diversificación también en el continente. Uno de ellos es el encontrado en los gecos pigopódidos australasiáticos, que después de adquirir una innovación clave (un fenotipo en forma de serpiente), entraron en dinámicas de diversificación comparables a los grupos insulares. Otro ejemplo destacado trabajado en esta tesis la diversidad encontrada dentro de la subespecie de geco Pristurus rupestris rupestris. Esta subespecie, en realidad, está formada por 14 especies altamente divergentes que diversificaron en las montañas del noroeste de Arábico, constituyendo uno de los casos más extremos de diversificación en vertebrados en Arabia.