Genetic drift and rapid evolution of viviparity in insular fire salamanders (Salamandra salamandra)

Abstract

Continental islands offer an excellent opportunity to investigate adaptive processes and to time microevolutionary changes that precede macroevolutionary events. We performed a population genetic study of the fire salamander (Salamandra salamandra), a species that displays unique intraspecific diversity of reproductive strategies, to address the microevolutionary processes leading to phenotypic and genetic differentiation of island, coastal and interior populations. We used eight microsatellite markers to estimate genetic diversity, population structure and demographic parameters in viviparous insular populations and ovoviviparous coastal and interior populations. Our results show considerable genetic differentiation (F(ST) range: 0.06-0.27), and no clear signs of gene flow among populations, except between the large and admixed interior populations. We find no support for island colonization by rafting or intentional/accidental anthropogenic introductions, indicating that rising sea levels were responsible for isolation of the island populations approximately 9000 years ago. Our study provides evidence of rapid genetic differentiation between island and coastal populations, and rapid evolution of viviparity driven by climatic selective pressures on island populations, geographic isolation with genetic drift, or a combination of these factors. Studies of these viviparous island populations in early stages of divergence help us better understand the microevolutionary processes involved in rapid phenotypic shifts.

Figure 1

Sampling design and distribution of Iberian S. salamandra subspecies. The ranges of Iberian S. salamandra subspecies are represented on the map on the right. S. s. bernardezi and western populations of S. s. fastuosa are viviparous. The map on the left shows sampling localities included in this study. Ovoviviparous populations are represented by black circles and viviparous populations by black stars.

Figure 2

Population structure and gene flow in focal populations of S. salamandra. The six genetic demes inferred in STRUCTURE are represented with different colors. Individual assignment to the six genetic demes is shown for each population (bottom panel). Blue arrows on the map identify the location of peninsular isthmuses and their elevation, likely resulting from sedimentation processes along the shore in the last 2000–3000 years.

Figure 3

Genetic diversity and historical demographics. Mean and 95% CIs of observed heterozygosity (H_O), effective population sizes (Θ) and growth rates (G) for each population.