The unexpected genetic mating system of the red‐backed toadlet (Pseudophryne coriacea): A species with prolonged terrestrial breeding and cryptic reproductive behaviour

Abstract

Molecular technologies have revolutionized our classification of animal mating systems, yet we still know very little about the genetic mating systems of many vertebrate groups. It is widely believed that anuran amphibians have the highest reproductive diversity of all vertebrates, yet genetic mating systems have been studied in <1% of all described species. Here, we use single nucleotide polymorphisms to quantify the genetic mating system of the terrestrial breeding red-backed toadlet Pseudophryne coriacea. In this species, breeding is prolonged (approximately 5 months), and males construct subterranean nests in which females deposit eggs. We predicted that females would display extreme sequential polyandry because this mating system has been reported in a closely related species (P. bibronii). Parentage analysis revealed that mating success was heavily skewed towards a subset of males (30.6% of potential sires) and that nearly all females (92.6%) mated with one male. In a high percentage of occupied nests (37.1%), the resident male was not the genetic sire, and very few nests (4.3%) contained clutches with multiple paternity. Unexpectedly, these results show that sequential polyandry is rare. They also show that there is a high frequency of nest takeover and extreme competition between males for nest sites, but that males rarely sneak matings. Genetic analysis also revealed introgressive hybridization between P. coriacea and the red-crowned toadlet (Pseudophryne australis). Our study demonstrates a high level of mating system complexity, and it shows that closely related anurans can vary dramatically in their genetic mating system.

Genetic benefits of extreme sequential polyandry in a terrestrial‐breeding frog

“…Interestingly, polyandry is extremely rare in P. coriacea (O'Brien et al. ), which raises the intriguing possibility that outbreeding depression has favored the evolution of two alternative mating systems in toadlets: (1) monandry, whereby stringent mate choice facilitates genetically compatible pairings, and (2) sequential polyandry, whereby mating with multiple males ameliorates the costs of incompatible pairings.…”

“…Furthermore, in a recent study using genomic tools to investigate mate choice in the red backed toadlet Pseudophryne coriacea, a sister species to P. bibronii, females preferred to mate with more related males (O'Brien 2019). Interestingly, polyandry is extremely rare in P. coriacea (O'Brien et al 2018), which raises the intriguing possibility that outbreeding depression has favored the evolution of two alternative mating systems in toadlets: (1) monandry, whereby stringent mate choice facilitates genetically compatible pairings, and (2) sequential polyandry, whereby mating with multiple males ameliorates the costs of incompatible pairings.…”

A genome‐wide search for local adaptation in a terrestrial‐breeding frog reveals vulnerability to climate change

“…Samples from most locations (Binnu, Chidlow, Dudinin, Flint plot, Mullewa, Ridgefield farm and Yalgoo) were collected during the 2016 autumn-winter breeding season. This population occurred only 10 km from the Yalgoo P. guentheri population and so was used to test for potential hybridization, as admixture between lineages can occur at species boundaries within this taxonomic group (O'Brien, Keogh, Silla, & Byrne, 2018). Given the short period between the temporal samples from Pinjar, they are unlikely to represent different generations, but were nonetheless included to have independent samples of the same population and test for genetic changes over 1 year.…”

“…On this basis, higher levels of inbreeding would be expected in our populations near the northern range edge, yet we observed the opposite pattern. Alternatively, the differences could arise via kin selection in southern populations, or due to differing levels of multiple mating, as implied by marked divergence of male reproductive traits in these same populations (Rudin-Bitterli, 2018), and recognition of complex and variable mating systems in congeners (O'Brien et al, 2018). Alternatively, the differences could arise via kin selection in southern populations, or due to differing levels of multiple mating, as implied by marked divergence of male reproductive traits in these same populations (Rudin-Bitterli, 2018), and recognition of complex and variable mating systems in congeners (O'Brien et al, 2018).…”

“…One explanation is that selection against inbred individuals is particularly strong in the northern populations, as inbreeding depression is more severe in more harsh environments (Miller, 1984). Alternatively, the differences could arise via kin selection in southern populations, or due to differing levels of multiple mating, as implied by marked divergence of male reproductive traits in these same populations (Rudin-Bitterli, 2018), and recognition of complex and variable mating systems in congeners (O'Brien et al, 2018).…”