Biparental care and the evolution of monogamy in amphibians
Monogamy, the mating system of only having one partner at a time, is generally rare within the animal kingdom and largely restricted to birds. Social monogamy is applied to pairs that remain together throughout their lives, but do not necessarily mate exclusively with one partner. Approximately 90% of birds are described as socially monogamous for although these pairs will remain with the same partner for life, many will seek to mate with other partners. Genetic monogamy, which refers to exclusive mating between two pairs, is rare within vertebrates. For example, only 25% of socially monogamous bird species are actually genetically monogamous. The evolution of genetic monogamy has been of interest to biologists for many decades and it is thought that biparental care, where both parents look after the offspring, has been an important factor in driving the evolution of monogamy. In species where biparental care is crucial for the offspring survival, working together results in greater survival of the young and greater reproductive output.
Parental care is generally rare within the amphibians and paternal care is considered to be the first form of parental care to have evolved. This is in contrast to birds and mammals, where maternal care appears to have evolved first. Within the amphibians parental care is often associated with tropical terrestrial species, particularly poison dart frogs belonging to the genus Ranitomeya. After females have laid their small clutches of eggs the males often carry the eggs to phytotelmata (pools of water in the axils of tree-dwelling plants) and exhibit egg-guarding. Biparental care has subsequently evolved where by females may lay non-fertile (or trophic) eggs in these small bodies of water to feed developing larvae. Known as trophic feeding, this form of maternal care has been reported from a range of terrestrial breeding tropical frog species and within the Ranitomeya, is associated with larvae developing in very nutrient poor, small bodies of water.
Recent research has shown that where biparental care has evolved in amphibian species, this has also resulted in the evolution of genetic monogamy. Prior to 2010, social and genetic monogamy had not been recorded in any species of amphibian. However, research by Brown et al. (2010) documented that social and genetic monogamy occurs in the mimic poison frog (Ranitomeya imitator) (Figure 1). This species occurs in north-central Amazonian Peru, in the regions of Loreto and San Martín and occurs in rainforest habitats between 200 and 1,200 m (Figure 2). Following courtship, the female mimic poison frog lays arboreal clutches of 1–3 eggs on understorey vegetation. The male guards the egg clutches and transports individual tadpoles on their backs to small phytotelmata. The female then lays trophic eggs into the water to provide food for the developing larvae. In an experimental study, Brown et al. (2010) found that 11 out of 12 pairs investigated showed genetic as well as social monogamy by the use of molecular markers. However, the closely related R. variabilis shows no monogamy and is highly promiscuous. In this species the male provides parental care but the female does not provide trophic eggs. Pairs preferred larger pools for tadpole deposition which contain higher levels of nutrients so additional trophic feeding by the female is less required (Brown et al., 2008). It appears that small pool size with low nutrient levels is crucial in driving the evolution of biparentral care and monogamy in species of poison dart frogs. Brown et al. (2010) experimentally confirmed the importance of trophic feeding by showing that tadpoles denied trophic eggs had lower growth rates than controls. Further experiments by Tumulty et al. (2016) demonstrated a significant reduction in reproductive success when males were removed after tadpole deposition, establishing the importance of male care for tadpole growth and survival throughout development. Therefore, because R. imitator breeds in small, low-nutrient waterbodies, both males and females are required to provide parental care. This requirement for active parental care from both the male and female appears to have driven the evolution of genetic monogamy and stable pair bonds in this species.
Many studies have shown that there are many advantages to biparental care but the high occurrence of extra pair matings, particularly in birds, indicates that there are many genetic advantages to having more than one mate. Therefore, why is the poison mimic frog so exclusively monogamous? The answer seems to lie in the importance of both male and female parental care in the pair bond. Experimental work on species where both partners are crucial for the survival of the young show that monogamy is strong, whereas in species where one partner is not obligatory, the level of monogamy is often weaker. This correlation suggests that genetic monogamy may be favoured when both male and female care is required for offspring survival. Results by Tumulty et al. (2016) indicate this to be the case in R. imitator, which has low rates (8.3%) of extra pair matings.
Overall, the biparental care hypothesis for promoting evolution of monogamy is gaining support from a variety of taxonomic groups and results from recent studies indicate that R. imitator shows a highly stable and cooperative long-term association between male and female and both care mutually for their offspring. The selection for long-term biparental care, as required by the demands of small, low nutrient pool size has driven the evolution of social and genetic monogamy in R. imitator.
Tumulty, J., Morales, V. & Summers, K. (2014) The biparental care hypothesis for the evolution of monogamy: experimental evidence in an amphibian. Behavioral Ecology, 25 (2): 262–270.
Brown, J.L., Morales, V. & Summers, K. (2008) Divergence in parental care, habitat selection and larval life history between two species of Peruvian poison frogs: an experimental analysis. Journal of Evolutionary Biology, 21: 1534–1543.
Brown, J.L., Morales, V. & Summers, K. (2010) A key ecological trait drove the evolution of biparental care and monogamy in an amphibian. The American Naturalist, 175 (4): 436-446.
IUCN SSC Amphibian Specialist Group (2014) Ranitomeya imitator. The IUCN Red List of Threatened Species 2014: e.T56378936A43715994. http://dx.doi.org/10.2305/IUCN.UK.2014-1.RLTS.T56378936A43715994.en. Downloaded on 11 August 2017.