Evolutionary Plasticity in Insular Lizard, Adapting over Reproduction, Metabolism, and Color Variation

Abstract

The Italian wall lizard (Podarcis siculus) living on islets exhibits a melanic skin coloration and a suite of adaptive traits lacking in nearby mainland populations. On islets, the unpredictable environmental conditions and highly fluctuating population densities are believed to have produced reversed island syndrome (RIS). Several physiological, behavioral, and life-history changes based on the RIS could result from positive selection on increased activity of melanocortins. We hypothesize that phenotypes on islets are the product of a plastic variation depending on the regulation of specific genes. Focusing on control systems that determine the insular-adapted phenotype, we demonstrated that reproductive markers, involved in the hypothalamus-hypophysis-gonadal axis, and metabolism markers, flags for hypophysis-melanocortin receptors, are all up-regulated in island lizards under the RIS. This behavior, combined with the observed limited variation in the mitochondrial genome, agrees with the hypothesis that plasticity enables populations to persist in novel environmental conditions and that over time, natural selection will "fine-tune" the population to the environment by modifying the phenotype under selection. We believe that analysis of the transcriptome and the single gene expression, such that all the variations observed in the island populations, can be useful to shed light on evolutionary plasticity as a process affecting animals' populations in general.

Keywords: Podarcis siculus; gene regulation; insularity; lizard; plasticity; transcriptome.

Figure 1

Study area and lizard phenotypes. The insets showed the geographical location of Scopolo, Faraglione of Capri (South Italy). (A) Lizard (Podarcis siculus siculus) showing a wild-type phenotype on mainland and (B) island lizard (Podarcis siculus coeruleus) with a blue melanic phenotype on Scopolo. Photos by Domenico Fulgione.

Figure 2

Heatmap of differentially expressed genes in the brain and testis of lizards from mainland and island lizards.

Figure 3

Volcano plot of differentially expressed genes from (A) the brain and (B) testis of island and mainland lizards. Negative values of logFC (fold changes) represent down-expressed genes, whereas positive values represent up-expressed genes in island samples. Red dots indicate differentially expressed genes with FDR (false discovery rate) < 0.005 and logFC > |2|.

Figure 4

Heatmap of 14 selected genes involved in the hypothalamus–hypophysis–gonadal axis. The gene expression in each sample is reported as log2 of the reads TMM.

Figure 5

Differential gene expression and plasmatic hormone levels indicative of phenotypic processes that reflect differences between island and mainland lizard populations. (A) qRT-PCR of the GNRH gene; (B) plasma levels of the dihydrotestosterone hormone (modified from [12]); (C) differential TMM expression of the gene for Leptin in brain; (D) differential TMM expression of the NPY gene in the brain; (E) differential TMM expression of the POMC gene in brain; (F) plasma levels of MSH hormone (modified from [12]).