The reduction in fecundity associated with the evolution of viviparity may have far-reaching implications for the ecology, demography, and evolution of populations. The evolution of a polygamous behaviour (e.g. polyandry) may counteract some of the effects underlying a lower fecundity, such as the reduction in genetic diversity. Comparing patterns of multiple paternity between reproductive modes allows us to understand how viviparity accounts for the trade-off between offspring quality and quantity. We analysed genetic patterns of paternity and offspring genetic diversity across 42 families from two modes of viviparity in a reproductive polymorphic species, Salamandra salamandra. This species shows an ancestral (larviparity: large clutches of free aquatic larvae), and a derived reproductive mode (pueriparity: smaller clutches of larger terrestrial juveniles). Our results confirm the existence of multiple paternity in pueriparous salamanders. Furthermore, we show the evolution of pueriparity maintains, and even increases, the occurrence of multiple paternity and the number of sires compared to larviparity, though we did not find a clear effect on genetic diversity. High incidence of multiple paternity in pueriparous populations might arise as a mechanism to avoid fertilization failures and to ensure reproductive success, and thus has important implications in highly isolated populations with small broods.
Multiple paternity is widespread in nature and despite costs, it has many associated benefits like increased genetic diversity and fertilization success. It has been described in many viviparous systems, suggesting the existence of some fitness advantages counteracting the inherent costs of viviparity, such as fecundity reduction and high parental investment. Reproductively polymorphic species, like the urodele Salamandra algira, which shows two types of viviparity: larviparity (i.e., delivering aquatic larvae), and pueriparity (i.e., delivering terrestrial metamorphosed juveniles), are suitable systems to study the relationship between reproductive modes and polygamous mating. Here, multiple paternity is confirmed in a pueriparous lineage of S. algira, as previously verified for the pueriparous lineages of the reproductively polymorphic species S. salamandra, suggesting polyandry is a successful mating strategy in pueriparous systems with reduced brood sizes. We discuss the potential benefits of polyandry in the context of viviparity evolution in urodeles.
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