Terrestrial reproduction and parental care drive rapid evolution in the trade-off between offspring size and number across amphibians

Abstract

The trade-off between offspring size and number is central to life history strategies. Both the evolutionary gain of parental care or more favorable habitats for offspring development are predicted to result in fewer, larger offspring. However, despite much research, it remains unclear whether and how different forms of care and habitats drive the evolution of the trade-off. Using data for over 800 amphibian species, we demonstrate that, after controlling for allometry, amphibians with direct development and those that lay eggs in terrestrial environments have larger eggs and smaller clutches, while different care behaviors and adaptations vary in their effects on the trade-off. Specifically, among the 11 care forms we considered at the egg, tadpole and juvenile stage, egg brooding, male egg attendance, and female egg attendance increase egg size; female tadpole attendance and tadpole feeding decrease egg size, while egg brooding, tadpole feeding, male tadpole attendance, and male tadpole transport decrease clutch size. Unlike egg size that shows exceptionally high rates of phenotypic change in just 19 branches of the amphibian phylogeny, clutch size has evolved at exceptionally high rates in 135 branches, indicating episodes of strong selection; egg and tadpole environment, direct development, egg brooding, tadpole feeding, male tadpole attendance, and tadpole transport explain 80% of these events. By explicitly considering diversity in parental care and offspring habitat by stage of offspring development, this study demonstrates that more favorable conditions for offspring development promote the evolution of larger offspring in smaller broods and reveals that the diversity of parental care forms influences the trade-off in more nuanced ways than previously appreciated.

The evolution of parental care in salamanders

“…Interestingly, we did not uncover associations between egg size, clutch size and parental care. Although associations between large eggs and parental care are assumed to be widespread among ectotherms 14 , 27 , 30 , they may be mediated by a common underlying factor, such as terrestrial reproduction 11 . In salamanders, the association between large eggs and terrestrial egg laying may not be straightforward since stream-type aquatic environments also select for large eggs 24 – 26 .…”

“…Our overall objective here is to explore the life history, climatic and reproductive correlates of parenting in salamanders. Whilst previous studies of salamander reproduction were insightful 10 , 23 – 27 , they left two main questions unresolved. First, we still do not know if parental care is associated with reproductive modes, in particular with the mode of fertilisation and various forms of offspring development.…”

“…larger reproductive investment into individual offspring by providing more nutrients that supply the developing embryo as indicated by large eggs 13 , 30 . Thus, we predicted that parental care is associated with large eggs and with small clutches owing to the trade-off between egg size and clutch size 13 , 22 , 27 , 30 . Finally, we also investigate the role of climate: based on previous studies, we predicted that harsh environment as indicated by less precipitation and/or uneven distribution of precipitation is associated with extensive parenting 16 , 17 , 31 , 32 .…”

The reproductive ecology drivers of egg attendance in amphibians

“…Because amphibian terrestrial eggs are large and laid in small clutches (Furness et al, 2022;Gomez-Mestre et al, 2012), their high fitness value is a likely driving force promoting the evolution of female egg attendance since female fitness is constrained by the number of eggs produced (Gomez-Mestre et al, 2012;Smith & Fretwell, 1974).…”

The evolution of reproductive modes and life cycles in amphibians

“…Occupation of new niche space can lead to ecological opportunity 26 and thus to increased diversification rates through reduced extinction and/ or increased speciation. Furthermore, increased terrestriality is generally accompanied by increased egg size, decreased clutch size, reduced body size 21 , and increased parental care 21,[27][28][29] . These changes, especially reduced body size, may reduce dispersal ability and thereby increase diversification, by increasing allopatric speciation 30,31 .…”