Fixation of genetic variation and optimization of gene expression: The speed of evolution in isolated lizard populations undergoing Reverse Island Syndrome

Abstract

The ecological theory of island biogeography suggests that mainland populations should be more genetically divergent from those on large and distant islands rather than from those on small and close islets. Some island populations do not evolve in a linear way, but the process of divergence occurs more rapidly because they undergo a series of phenotypic changes, jointly known as the Island Syndrome. A special case is Reversed Island Syndrome (RIS), in which populations show drastic phenotypic changes both in body shape, skin colouration, age of sexual maturity, aggressiveness, and food intake rates. The populations showing the RIS were observed on islets nearby mainland and recently raised, and for this they are useful models to study the occurrence of rapid evolutionary change. We investigated the timing and mode of evolution of lizard populations adapted through selection on small islets. For our analyses, we used an ad hoc model system of three populations: wild-type lizards from the mainland and insular lizards from a big island (Capri, Italy), both Podarcis siculus siculus not affected by the syndrome, and a lizard population from islet (Scopolo) undergoing the RIS (called P. s. coerulea because of their melanism). The split time of the big (Capri) and small (Scopolo) islands was determined using geological events, like sea-level rises. To infer molecular evolution, we compared five complete mitochondrial genomes for each population to reconstruct the phylogeography and estimate the divergence time between island and mainland lizards. We found a lower mitochondrial mutation rate in Scopolo lizards despite the phenotypic changes achieved in approximately 8,000 years. Furthermore, transcriptome analyses showed significant differential gene expression between islet and mainland lizard populations, suggesting the key role of plasticity in these unpredictable environments.

Gut microbiota plasticity in insular lizards under reversed island syndrome

“…MA populations showed lower level of Oscillospira than IL, and this decreased after food providing but with slight variation if compared to IL microbiota. Arguably, the differential level of Oscillospira and variations in a shorter time interval than mainland conspecifics are in agreement with RIS 23 .…”

“…The short distance between the island and the mainland allows for the existence of a moderate gene flow between the two populations, excluding important phenomena of genetic drift 38 . Therefore, we believe that this character is caused by the RIS as reported in some of our papers 18 , 19 , 22 , 23 .

Figure 1 Study area and lizard phenotypes.

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“…However, it should also be considered that these two groups shared 77% of the microbial bacterial groups. These results could be an evidence of the ability of the island lizards (under RIS) to respond more significantly than mainland populations to drastic and unexpected changes, by adopting adaptive plasticity mechanisms 11 , 21 , adding another important element to the theoretical basis of the syndrome 18 , 19 , 22 , 23 .…”

“…An interesting island model system is represented by populations of lizards living on small islands close to the mainland, undergoing the Reverse Island Syndrome (RIS) 18 , 19 for which rapid phenotypic changes are often visible in a short time 20 , in our interpretation, due to genome plasticity (sensu 21 ) based on differential expression of some genes 22 , 23 .…”

Correction: Fixation of genetic variation and optimization of gene expression: The speed of evolution in isolated lizard populations undergoing Reverse Island Syndrome

“…The erroneously included description of the skeletochronology is adapted from reference [24], which is cited in support of the snout-vent length methodology used to select adult lizards [ 1 ].…”