Abstract

The adaptive significance of sequential polyandry is a challenging question in evolutionary and behavioral biology. Costs and benefits of different mating patterns are shaped by the spatial distribution of individuals and by genetic parameters such as the pairwise relatedness between potential mating partners. Thus, females should become less choosy as costs of mating and searching for mates increase. We used parentage assignments to investigate spatial and genetic patterns of mating across a natural population of the Neotropical frog Allobates femoralis, a species characterized by male territoriality and care and female iteroparity. There was no correlation between genetic and spatial distances between adult individuals across the population. In 72% of cases, females mated with males available within a radius of 20 m. Mean pairwise relatedness coefficients of successful reproducers did not differ from random mating but had a lower variance than expected by chance, suggesting maximal reproductive output at intermediate genetic divergence. We also found evidence for selection in favor of more heterozygous individuals between the embryo and adult stage. The level of sequential polyandry significantly increased with the number of spatially available males. Females that had more candidate males also produced more adult progeny. We hypothesize that the benefits associated with female multiple mating outweigh the costs of in- and outbreeding depression, and consequently precluded the evolution of ‘choosy’ mate selection in this species.

Highlights

  • A key target in evolutionary biology is to determine the costs and benefits of specific mating patterns that have led to the wide range of animal mating systems

  • In the present study we investigated spatial and genetic patterns of reproductive success across a natural population of the Neotropical frog A. femoralis

  • The variance in pairwise relatedness of successful reproducers was smaller than expected from random mating, suggesting that reproductive success is highest between pairs of intermediate genetic divergence

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Summary

Introduction

A key target in evolutionary biology is to determine the costs and benefits of specific mating patterns that have led to the wide range of animal mating systems. In nonresource-based systems, genetic quality in terms of ‘good’ or ‘compatible’ genes often constitutes an important factor regarding mate choice [1,2]. Both systems can lead to the evolution of restrictive (i.e. choosy) mating, resulting in high reproductive skew in the non-choosing sex, and to polyandry, a common mating system despite associated costs for females [3]. In cases where high levels of matings among close relatives result in a substantial reduction in overall population fitness due to inbreeding depression (for a review see [4]; see [5,6,7]), a preference for unrelated partners in the choosing sex can constitute a strong selective benefit. At the other side of the spectrum, mating with very distantly related individuals can have negative fitness consequences (outbreeding depression; [8,9])

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