Evolutionary causes and consequences of sequential polyandry in anuran amphibians

Abstract

Among anuran amphibians (frogs and toads), there are two types of polyandry: simultaneous polyandry, where sperm from multiple males compete to fertilize eggs, and sequential polyandry, where eggs from a single female are fertilized by multiple males in a series of temporally separate mating events, and sperm competition is absent. Here we review the occurrence of sequential polyandry in anuran amphibians, outline theoretical explanations for the evolution of this mating system and discuss potential evolutionary implications. Sequential polyandry has been reported in a limited number of anurans, but its widespread taxonomic and geographic distribution suggests it may be common. There have been no empirical studies that have explicitly investigated the evolutionary consequences of sequential polyandry in anurans, but species with this mating pattern share an array of behavioural, morphological and physiological characteristics, suggesting that there has been common sexual selection on their reproductive system. Sequential polyandry may have a number of adaptive benefits, including spreading the risk of brood failure in unpredictable environments, insuring against male infertility, or providing genetic benefits, either through good genes, intrinsic compatibility or genetic diversity effects. Anurans with sequential polyandry provide untapped opportunities for innovative research approaches that will contribute significantly to understanding anuran evolution and also, more broadly, to the development of sexual-selection and life-history theory.

Evolution of sperm morphology in anurans: insights into the roles of mating system and spawning location

“…Following Byrne and Roberts [47], we used mating system as an imperfect surrogate for the intensity of sperm competition on a two-point scale: 1 = simultaneous polyandry, where multiple males clasp a female and sperm from males to simultaneously compete to fertilize eggs over the course of a breeding season; 2 = monandry, where a female mates with one male over the course of a breeding season and deposits a single clutch. In Chaparana quadrana we observed that multiple males participated in fertilising the eggs deposited by a single female without amplexus (similar to C. taihangnicus ) [48], and we regarded this species as simultaneously polyandrous.…”

Short Amplexus Duration in a Territorial Anuran: A Possible Adaptation in Response to Male-Male Competition

“…The usual adaptive explanation is that prolonged mating in internally fertilizing animals acts as a form of post-insemination mate guarding to prevent re-insemination of females and to increase sperm loading under intense sperm competition [9,15]. This adaptive function, however, is not particularly well suited for externally fertilizing animals (but see 59,60) and cannot explain our findings. Because female R. adenopleura deposit their eggs in one bout in a relatively short period of time, and males fertilize eggs upon their release, mate guarding is not necessary to prevent females from re-mating or to decrease the intensity of sperm competition.…”

Sexual size dimorphism in anurans: roles of mating system and habitat types

“…This pattern is contradictory to the well-established concept that male-male competition (sexual selection) drives to increase male body size and results in male-biased SSD [1]. Several potential causes can explain why intensity of sexual selection does not promote evolution of SSD in anurans [1,11,15,19]. Firstly, mating success is positively correlated with male body size in some species, but not in others.…”

“…wetlands, grasslands, steams, trees and ponds) and exhibit a remarkable diversity of mating system (i.e. social polyandry and social monogamy) that is unique among vertebrates [10,11]. If the selection hypotheses are valid, we expect mating system and habitat types having effects on SSD in anurans.…”