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

['Andrew I. Furness', 'Department Of Biological', 'Marine Sciences', 'University Of Hull', 'Hull', 'United Kingdom', 'Energy', 'Environment Institute', 'Chris Venditti', 'School Of Biological Sciences']

Date: 2022-01 

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.

Citation: Furness AI, Venditti C, Capellini I (2022) Terrestrial reproduction and parental care drive rapid evolution in the trade-off between offspring size and number across amphibians. PLoS Biol 20(1): e3001495. https://doi.org/10.1371/journal.pbio.3001495 Academic Editor: Michael D. Jennions, The Australian National University, AUSTRALIA Received: June 18, 2021; Accepted: November 26, 2021; Published: January 4, 2022 Copyright: © 2022 Furness et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability: The authors confirm that all data underlying the findings are fully available without restriction. The dataset compiled and analysed for this manuscript has been uploaded as S1 Data. The sources for the data are available in S1 Data and list in S3 Data. The phylogeny pruned from Pyron (2014) and used for the analysis is uploaded as S2 Data. Funding: We thank the University of Hull and Queen’s University Belfast for supporting this project with funding to IC, and Leverhulme Trust (Research Project Grant RPG-2017-017 to CV) for funding this research. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Leverhulme Trust: https://www.leverhulme.ac.uk. Competing interests: The authors have declared that no competing interests exist. Abbreviations: ESS, effective sample size; MCMC, Markov chain Monte Carlo; PGLS, phylogenetic generalized least squares; VIF, variance inflation factor

Discussion The trade-off between offspring size and number is central to life history theory and has important implications in both basic and applied questions; however, which selective pressures influence its evolution, is debated. Here, we have investigated 2 hypotheses proposing that parental care and/or more favorable terrestrial habitats for offspring development select for larger eggs [13,39,40,52], while accounting for allometric effects, direct development, and the trade-off with clutch size. We have also asked whether the proposed drivers have acted on clutch size rather than egg size. Our results show that amphibians with direct development and those with terrestrial offspring have both larger eggs and smaller clutches (Fig 3). Considering individual parental care forms separately has allowed us to unravel the complex and contrasting influence that they exert on the trade-off, with egg brooding, male and female egg attendance increasing egg size, female tadpole attendance and feeding decreasing egg size, and egg brooding, tadpole feeding, male tadpole attendance, and male tadpole transport reducing clutch size (Fig 3). Importantly, by simultaneously considering variation in rates of phenotypic evolution across the phylogeny, our variable rates analyses demonstrate that the significant predictors of egg and clutch size evolution can explain much of the rapid phenotypic change in these life history traits, indicating that they have imposed intense selection on the offspring size–number trade-off. PPT PowerPoint slide

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TIFF original image Download: Fig 3. Summary of results on the evolution of egg size–clutch size trade-off. (A) Distribution of parental care forms, offspring habitat, direct development, and life history traits in amphibians (n = 805 species; raw data in S1 and S2 Data). All variables, except clutch size, egg size, and body size, are binary. (B) Summary of the significant associations for the trade-off between egg size and clutch size, combining their respective reduced models (S3B and S3D Table). Variables associated with increases in egg or clutch size are above the trade-off and indicated with a plus; variables associated with decreases in egg or clutch size are below the trade-off and indicated by a minus. For each variable, we report in brackets the percentage of change in egg or clutch size computed for an average-sized amphibian with average clutch size or egg size, respectively (S4A Table for egg size and S4B Table for clutch size). https://doi.org/10.1371/journal.pbio.3001495.g003 We find broad support for theoretical models that both parental care and terrestrial offspring habitat promote the evolution of larger offspring, but the role of parental care is more complex than previously appreciated and depends on the type of care, the stage at which care is provided and the sex of the caring parent. Specifically, while accounting for allometry and the trade-off with clutch size, our study demonstrates that eggs are larger by about 20% if terrestrial, as predicted by theoretical models suggesting that favorable environmental conditions for offspring development select for larger offspring [40]. In support of the theoretical prediction that parental care drives an increase in egg size [52], we simultaneously find that eggs are 15% and 20% larger if attended by females and males, respectively, and nearly 60% bigger if brooded by parents. However, in contrast to this prediction [52], eggs are smaller by 32% with tadpole feeding and by nearly 50% with female tadpole attendance. Although these results may seem unexpected, we note that Nussbaum and Schultz’s theoretical model [40] predicts that, at any given level of parental care, egg size may decrease if environmental conditions for juvenile survival improve. We propose that this may be the case for female tadpole attendance, which occurs in ponds and terrestrial protected habitats, such as burrows, where the tadpoles can be defended against predators [39,73]. We suggest that tadpole feeding females may not need to produce large eggs because they continue to provision their young throughout larval development, analogous to matrotrophic viviparous fish (for example, those with maternal provisioning of offspring via a placenta). Oviparous and viviparous species without matrotrophy typically supply their eggs fully before fertilization, after which they provide no further nutrition [74,75]. Conversely, females of matrotrophic fish start off with small eggs, which they continue to provision throughout development [74,75]. Overall, accounting for diversity in parental care has allowed us to unravel that different care behaviors and adaptations may drive the evolution of egg size in different directions and at different magnitude. We anticipate that similar results will be found in taxa with high diversity of care forms, such as other vertebrate classes, insects, and crustaceans. Theoretical models and empirical studies on the role of care and offspring habitat have primarily focused on the evolution of offspring size alone [14,15,40,52,53]. However, selection may act on offspring number instead and only indirectly alter offspring size. While accounting for offspring number in statistical models offers a much stronger test of hypotheses on proposed drivers of offspring size evolution, investigating whether such drivers also affect offspring number (while accounting for offspring size) provides a comprehensive answer. We thus also ask whether the proposed drivers of egg size evolution directly affect clutch size. After accounting for allometry and the trade-off with egg size, our variable rates analysis indicates that terrestrial habitat at the egg and larval stage, direct development, egg brooding, tadpole feeding, male tadpole attendance, and male tadpole transport are associated with a substantial reduction in clutch size ranging between 50% and 70%. These results are consistent with numerous physiological and physical mechanisms known to constrain clutch size. For example, because oxygen diffusion is compromised within the jelly of terrestrial eggs, smaller clutches ensure sufficient oxygenation by reducing competition [46]. Oxygen limitation is likely to also be particularly acute for direct developing eggs, typically laid on land, given their extended period of development and large size. For tadpole feeding, we suggest that mothers cannot support large clutches because they often provide energetically expensive nutrition over a long period of offspring development. Consistent with this idea, female strawberry poison frogs (Oophaga pumilio) lay fewer eggs when simultaneously provisioning older tadpoles, while tadpoles in larger clutches receive smaller meals and suffer higher mortality [76]. Instead, physical space may constrain clutch size in brooding species, in species with male tadpole transport, and those with terrestrial tadpoles. Specifically, the size of the body cavity or surface area of the back is likely to limit the number of eggs parents can care for in egg brooding frogs or the number of tadpoles that males can transport [73]. Likewise, terrestrial tadpoles with no caring parents frequently develop in foam nests, burrows, or within cup-shaped nests and typically do not feed [39,64]. These confined spaces are likely to provide shelter to only a few tadpoles, while limitation to oxygen diffusion might further constrain the number of developing larvae as it does for eggs. While constraints on offspring number beyond amphibians have been previously discussed mostly in relation to viviparity [11,77], our results suggest that clutches are likely to be reduced in many other species in which the eggs or young are physically associated with the parental body or are placed in microenvironments or nests where physiological or physical conditions impose an upper limit to the number of offspring they can accommodate. Bringing findings for egg size and clutch size together, this study reveals how proposed drivers affect both or only one of the 2 elements of this trade-off (Fig 3B). Specifically, terrestrial eggs, egg brooding, and direct development act simultaneously on both egg and clutch size, i.e., directly increase egg size and decrease clutch size, beyond the indirect effect that they already have on the other element of the trade-off. Instead, male egg attendance, female egg attendance, and female tadpole attendance only associate with egg size; tadpole terrestriality, male tadpole attendance, and male tadpole transport only associate with smaller clutches; while tadpole feeding is associated with both smaller eggs and smaller clutches. By accounting for diversity in care forms and offspring habitat by stage of development, we demonstrate that terrestrial habitat and direct development consistently lead to larger eggs and smaller clutches, while different care forms can have contrasting effects on the offspring size–number trade-off. Thus, it is not surprising that studies clumping or arbitrarily ranking care forms across developmental stages find that terrestrial habitat, but not parental care, is associated with egg size or number. Many theoretical models consider parental care as a uniform species characteristic that varies in duration, intensity (for example, how much food to provision), or, in the context of sexual conflict, by caring sex. However, our study demonstrates that the effect of parental care on egg size and clutch size is far more complex and differs depending on the type of care, the stage at which care is given and the sex of the carer. We thus need a new theoretical framework that explicitly considers such diversity of care and provides quantitative predictions on how different care behaviors and adaptations should impact the evolutionary trajectory of egg and clutch size and, more broadly, life history strategies. Importantly, our variable rates models explicitly consider heterogeneity in rates of phenotypic evolution and simultaneously identify where in the phylogeny egg size and clutch size have accumulated more phenotypic change than expected, indicative of intense selection. Episodes of exceptional rates of egg size evolution are few (19 branches), and the significant ecological and parental care predictors account for only 3 of these exceptional rates. In contrast, exceptional rates of evolution in clutch size were frequent (135 branches), and 80% of these were explained by ecological and parental care predictors. Thus, our approach reveals that many more branches across the phylogeny exhibit higher rates of phenotypic evolution for clutch size than egg size, most of which is explained by offspring habitat, direct development, and care forms. This likely reflects the potential physiological constraints on the size of anamniotic eggs (for example, due to oxygenation [46,47]) and the higher interspecific variance in clutch size (ranging from 1 to tens of thousands) than egg size. Therefore, our study reveals that there is greater opportunity for selection on clutch size than egg size in amphibians. Based on our findings, we expect that selection has acted more strongly on offspring number than on offspring size in lineages with high diversity of parental care forms and adaptations, high diversity of habitats in which the eggs develop, and large variance in clutch size, like fish and insects. Conversely, egg size may be under stronger selection than clutch size in lineages like birds that exhibit lower diversity in care forms compared to amphibians and are limited in the number of offspring they can produce due space limitations within nests. We suggest that future comparative studies testing hypotheses on the evolutionary drivers of this key life history trade-off consider both offspring number and size and explicitly incorporate diversity in parental care, while theoretical models should evaluate under which conditions the greater response of clutch size to selection affects the evolutionary trajectory of offspring size. To conclude, this study demonstrates that evolutionary changes in offspring habitat, parental care, and direct development have led to rapid adaptive evolution in egg and clutch size. While terrestrial offspring habitat influences the offspring size–number trade-off as predicted by theoretical models [13,39,40,52], considering the full diversity in care forms by stage of offspring development and sex of caring parent has revealed that different care behaviors and adaptations have contrasting effects on the trade-off. Importantly, incorporating variation in rates of egg and clutch size evolution in our theoretical framework has allowed us to test predictions not only on the direction and magnitude of effects of proposed drivers, but also on how proposed drivers lead to rapid change in the trade-off. Our approach thus reveals that episodes of rapid evolution in egg and clutch size are explained by offspring habitat, direct development, and some care forms, as expected if these traits select for rapid adaptive changes in egg and clutch size to new conditions. More broadly, we expect that other comparative studies incorporating rate heterogeneity in their theoretical and analytical framework will further reveal how behavioral traits and ecological conditions explain rapid phenotypic change, and thus identify episodes of intense selection, at a large comparative scale.

Acknowledgments We thank Joanna Baker for sharing her R code; VIPER High Performance Computing facility and its support team at the University of Hull; James Gilbert for comments on early results of this study; and David Reznick, Martha Crump, and Jesse Delia for comments on an earlier draft of this manuscript.

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