The evolution of viviparity in holocene islands: ecological adaptation versus phylogenetic descent along the transition from aquatic to terrestrial environments

Abstract

Species that contain populations with different reproductive modes offer excellent opportunities to study the transition between such strategies. Salamandra salamandra (Linnaeus, 1758) is one of two species within the Salamandra-Lyciasalamandra clade which displays two reproductive modes simultaneously. Along the S. salamandra distribution, the common reproductive mode is ovoviviparity although the species also has viviparous populations in the northern Iberian Peninsula. The occurrence of viviparity has recently been reported in two small offshore island populations on the Atlantic coast (NW Iberia), which originated after the last glacial period (8000-9000 years ago). In this paper, we analysed ovoviviparous, hybrid and viviparous populations (inland and mainland) from 17 localities across the northern Iberian Peninsula using two mitochondrial markers (Cyt b and COI, c. 1100 bp). Phylogenetic and phylogeographic analyses highly support that viviparity arose as an evolutionary novelty in the S. salamandra island populations and that viviparous populations are therefore not monophyletic. The recent insularity of Atlantic island populations leads us to conclude that the transition from ovoviviparity to viviparity can happen in a very short-time span. Additionally, to determine the likely source of this evolutionary transition, we discuss how ecological pressures could have an effect on the maintenance of the ovoviviparous reproductive mode. Hence, taking into account the results of this study, we propose the consideration of the island populations as an evolutionary unit for conservation purposes.

Biogeography and contemporary climatic differentiation among Moroccan Salamandra algira

“…This striking divergence, probably related to environmental pressures within the distribution of S. a. tingitana, again demonstrate the particularly high tendency for adaptive differentiation and speciation (sensu e.g. Steinfartz, Weitere & Tautz, 2007;Velo-Antón et al, 2007) within the genus Salamandra.…”

“…As in other examples, the viviparous reproductive behaviour found in the form of S. a. tingitana north of the Oued Martil could be caused by environmental pressures (e.g. Gasser & Joly, 1972;Velo-Antón et al, 2007), as hypothesized by Donaire- , although the exact origin is unknown.…”

“…As suggested by Velo-Antón et al (2007), the absence of surface water on karstic limestone soils can rapidly influence the transition of reproductive behaviour in Salamandra (within less than 10 000 years). There is little or no natural surface water north of the Oued Martil, and, if present, it is seldom used to deposit larvae (Donaire- .…”

Evolution of Viviparity in Salamanders (Amphibia, Caudata)

“…Viviparous and ovoviviparous individuals are in contact and can mate and reproduce, providing an unusual and exceptional natural scenario for studying the evolution of reproductive strategies within the group from a population perspective (García-París et al, 2003;Buckley et al, 2007;Buckley et al, 2009). Furthermore, the occurrence of viviparity has recently being reported in some insular populations of the subspecies S. s. gallaica (Velo-Antón et al, 2007). The evolutionary origin of these populations and, hence, of viviparity is different from the case described above for S. s. bernardezi and S. s. fastuosa, providing a second natural setting to study the evolution of viviparity in S. salamandra.…”

“…The evolutionary origin of these populations and, hence, of viviparity is different from the case described above for S. s. bernardezi and S. s. fastuosa, providing a second natural setting to study the evolution of viviparity in S. salamandra. Little is known, however, about the physiological and developmental characteristics of viviparity in this insular group, although it is likely related to the absence of water points in the islands (Velo-Antón et al, 2007). The occurrence of viviparity has also been reported recently in S. algira.…”