4.1. Genetic diversity of P. lilfordi: evolution in islands and population conservation
A fundamental goal in population ecology and evolution is to understand the processes that maintain genetic diversity, and those that drive intraspecific/interpopulation divergence across geographic space and time (Avise, 2000). In small insular populations, free of predators and with no immigrants, genetic diversity is primarily driven by genetic drift (due to environmental and demographic stochasticity, both particularly important in tiny islets) and density-dependent selection due to competition for the limited local resources (Hoffmann et al., 2021; Hunt et al., 2022; Travis et al., 2023). Founder effect and high inbreeding levels are also expected to further reduce the population genetic variance and accelerate the process of divergence from the original source population (Keller and Waller, 2002). Each P. lilfordi island clearly hosted a distinct population (all Fst distances were significant), with no contemporary gene flow (no recent translocations detected). Few small islets showed a remarkably high differentiation from all other islets (i.e. Porros and en Curt, Fst >0.2 for all pairs, see Figure 4), indicating either a strong founder effect and/or intense local drift and selection due to their reduced island size (Sendell‐Price et al., 2021). Despite being effectively closed, P. lilfordi populations harbored relatively high genetic diversity (Ho>0.09 and Pi> 0.1 for all populations), even higher than other continental and insular species of Podarcis (Sabolić and Štambuk, 2021). Diversity was overall largely comparable among all 16 populations studied and across their range of distribution (Figure 1 and Figure 3); nonetheless, association analyses supported the expected pattern of decreasing genetic diversity with decreasing island size (Furlan et al., 2012). Smaller islands also presented the highest number of private alleles, indicative of an ongoing process of differentiation. Mallorca/Cabrera archipelago typically hosted a higher genetic diversity than Menorca (Figure 3), with the islands of Cabrera, Guardia and Moltona (South of Mallorca) currently harboring the largest genetic diversity present in this species.
As previously reported by Bassitta et al . (2021), we also observed low levels of inbreeding for most populations (Fis< 0.08), even for tiny islets such as Esclatasang, Foradada, Porros, Revells and en Curt (all with Area< 0.7 ha, Fis<0.5, Table 1 and Figure 3). While small populations are expected to show a reduced heterozygosity (Keller and Waller, 2002), Fis values in P. lilfordi indicated a slight trend of positive increase with increasing islet surface, with the highest estimate found for the island of Moltona (Fis =0.16). A small inbreeding coefficient, negatively associated with island size, was also found in a previous study based on microsatellites from the three neighboring populations of Moltona, Na Guardia and en Curt (Rotger et al., 2021). A potential explanation is the existence of a population spatial substructure within larger islands, which would cause a non-random mating of individuals effectively reducing the observed heterozygosity. Nonetheless, we invite caution in interpretation of these results as SNP-based estimation of the inbreeding depression in wild populations is notoriously challenging (Schmidt et al., 2021) and would require pedigree-studies for a reliable quantification (Kardos et al., 2016).
Both the relatively high genetic diversity and low Fis values observed in P. lilfordi would suggest the existence of potential mechanisms for buffering inbreeding depression in these lizard populations, increasing their chances of persistence. In line with this, recent studies support the ability of insular lizards to counteract genetic depletion even in presence of a strong founder effect (see Sherpa et al., 2023).