Do female amphibians and reptiles have greater reproductive output if they have more mates?

Abstract

In general, males mate with multiple females to increase individual reproductive success. Whether or not, and under what circumstances, females benefit from multiple mating has been less clear. Our review of 154 studies covering 184 populations of amphibians and reptiles showed that polyandry was widespread and variable among and within taxonomic groups. We investigated whether amphibian and reptile females had greater reproductive output as the number of sires for offspring increased. Meta-analysis revealed significant heterogeneity in the dataset of all taxa. Expected heterozygosity was a significant moderator (covariate) of positive relationships between female reproductive output and the number of sires, but a sensitivity test showed the result was tenuous. Significant heterogeneity remained despite controlling for expected heterozygosity and other variables but was resolved for most taxonomic groups with subgroup meta-analyses. Subgroup meta-analyses showed that only female salamanders (Caudata) had significantly greater reproductive output with an increased number of sires. For many species of Caudata, males cannot coerce females into accepting spermatophores. We therefore suggest that if females control the number of matings, they can use polyandry to increase their fitness. Caudata offers ideal models with which to test this hypothesis and to explore factors enabling and maintaining the evolution of female choice. Outstanding problems may be addressed by expanding taxonomic coverage and data collection and improving data reporting. Significance Statement Many factors and combinations of factors drive polyandry. Whether or not females benefit from mating with more than one male remains equivocal. Focusing on amphibians and reptiles, our analyses demonstrate that female salamanders produced more offspring when mated with multiple males, whereas this was not the case for reptiles. Unlike many other species in our dataset, the polyandrous female salamanders fully control sperm intake and have chosen to mate multiple times. We further highlight problems and key directions for future research in the field.

Multiple paternity is related to adult sex ratio and sex determination system in reptiles

“…This proposition has been supported by within-species studies of reptiles showing that clutches fertilized by multiple males had higher genetic diversity and offspring viability than single-sired clutches (Fitze et al, 2005;Noble et al, 2013;Olsson & Madsen, 2001). However, a recent meta-analysis investigating female benefits from multiple mating in reptiles showed that female reproductive output did not increase consistently with increasing number of sires (Lee et al, 2022).…”

“…This proposition has been supported by within‐species studies of reptiles showing that clutches fertilized by multiple males had higher genetic diversity and offspring viability than single‐sired clutches (Fitze et al, 2005; Noble et al, 2013; Olsson & Madsen, 2001). However, a recent meta‐analysis investigating female benefits from multiple mating in reptiles showed that female reproductive output did not increase consistently with increasing number of sires (Lee et al, 2022). Alternatively, according to the second explanation, multiple paternity in reptiles may be driven more by males than by females: males may force copulations more frequently when females are scarce, as their chances of finding a receptive female is low.…”

Introduction to topical collection “Measuring individual reproductive success in the wild”

“…In many taxa, other than mammals or birds, newborn offspring cannot be marked, limiting research on survival to measuring clutch size. Although many studies have genetically assigned offspring to mothers and fathers in amphibians and reptiles (Lee et al 2022), very few have monitored offspring after they leave the nest or laying site. Similarly, the availability of fitness data for fishes and most invertebrates is sparse, with significant exceptions highlighted in this issue, such as the sponge-dwelling goby (Francis et al 2022).…”

“…Multiple paternity within the same clutch or litter is widespread in amphibians and reptiles. Although it is often inferred that such genetic diversity benefits females, this is true only for salamanders, among the 7 clades with 184 populations of amphibians and reptiles that were examined (Lee et al 2022). Because males cannot coerce female salamanders to accept spermatophores, the authors suggest female choice is critical to the relationship between polyandry and fitness.…”