The global macroecology of brood size in amphibians reveals a predisposition of low‐fecundity species to extinction

Abstract

Aim The diversity of brood size across animal species exceeds the diversity of most other life‐history traits. In some environments, reproductive success increases with brood size, whereas in others it increases with smaller broods. The dominant hypothesis explaining such diversity predicts that selection on brood size varies along climatic gradients, creating latitudinal fecundity patterns. Another hypothesis predicts that diversity in fecundity arises among species adapted to different microhabitats within assemblages. A more recent hypothesis concerned with the consequences of these evolutionary processes in the era of anthropogenic environmental change predicts that low‐fecundity species might fail to recover from demographic collapses caused by rapid environmental alterations, making them more susceptible to extinctions. These hypotheses have been addressed predominantly in endotherms and only rarely in other taxa. Here, we address all three hypotheses in amphibians globally. Location Global. Time period Present. Major taxa studied Class Amphibia. Methods Using a dataset spanning 2,045 species from all three amphibian orders, we adopt multiple phylogenetic approaches to investigate the association between brood size and climatic, ecological and phenotypic predictors, and according to species conservation status. Results Brood size increases with latitude. This tendency is much stronger in frogs, where temperature seasonality is the dominant driver, whereas salamander fecundity increases towards regions with more constant rainfall. These relationships vary across continents but confirm seasonality as the key driver of fecundity. Ecologically, nesting sites predict brood size in frogs, but not in salamanders. Finally, we show that extinction risk increases consistently with decreasing fecundity across amphibians, whereas body size is a “by‐product” correlate of extinction, given its relationship with fecundity. Main conclusions Climatic seasonality and microhabitats are primary drivers of fecundity evolution. Our finding that low fecundity increases extinction risk reinforces the need to refocus extinction hypotheses based on a suggested role for body size.

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

“…Answering this question is fundamental not only for advancing theory, but also because these life history traits influence the demographic trajectory of natural and introduced populations [ 21 – 25 ] and their ability to overcome many anthropogenic stressors [ 24 , 26 – 28 ]. For example, in several taxa, fecundity influences extinction risk [ 27 , 29 ], population growth rate [ 30 ], invasion success [ 21 , 22 ], and the ability to thrive in urban, or more generally human-modified, habitats [ 26 , 28 ]. Here, we test hypotheses predicting that parental care or terrestrial habitats in which offspring develop alter the offspring size–number trade-off, specifically leading to smaller clutches of larger eggs, in a sample of over 800 amphibian species.…”

“…Offspring number rather than offspring size may, however, be the target of selection. Environmental conditions can drive brood size evolution [ 19 , 27 ] since they determine the mortality risks on eggs and young, for example, due to predation, desiccation, thermoregulation, or oxygen availability [ 17 , 20 , 54 , 55 ], and the amount of resources available to females for provisioning their eggs and young posthatching/birth in caring species [ 17 ]. Discovering which trait in the trade-off is under selection is thus not trivial because reasons as to why females should invest in larger or in more offspring may differ and a change in one of the traits in the trade-off does not always lead to a proportional change in the other.…”

“…Similarly, selection in reef fishes has acted differently on egg size and clutch size [ 18 ]. Specifically, demersal guarded eggs are larger than pelagic and scattered eggs as predicted by theoretical models of parental care evolution [ 13 , 52 , 53 ], while clutches are bigger in larger species, likely reflecting fecundity selection [ 19 , 27 ], but clutch size is unrelated to egg size. To identify whether selection by a proposed driver alters offspring size and/or offspring number, both elements of the trade-off, needs to be considered.…”

IUCNN – Deep learning approaches to approximate species' extinction risk

“…Although the RL is designed for applied conservation, the standardized assessment across regions and taxa makes it a widely used resource for biogeographic and (macro)ecological research. For instance, RL extinction risk assessments have been used to relate traits, such as body mass, to species extinction risk (Boehm et al, 2016;Pincheira-Donoso et al, 2021;Richards et al, 2021;Rolland & Salamin, 2016), to quantify the effect of threats, such as agriculture, on species extinction risk (Polaina et al, 2018), to quantify links between species extinction risk and invasive species (Tingley et al, 2016;Walsh et al, 2012), to characterize the distribution of threatened species (Coll et al, 2015), to predict future biodiversity losses (Andermann et al, 2021;Monroe et al, 2019) and to understand the potential effects of extinction on large-scale diversity patterns (Oliveira et al, 2020;Smiley et al, 2020).…”

IUCNN - deep learning approaches to approximate species’ extinction risk

“…Although the RL is designed for applied conservation, the standardized assessment across regions and taxa make it a valuable and widely-used resource for biogeographic and (macro)ecological research. For instance, RL extinction risk assessments have been used to relate traits, such as body mass, to species extinction risk (Boehm et al, 2016; Pincheira□Donoso et al, 2021; Richards et al, 2021; Rolland & Salamin, 2016), to quantify the effect of threats, such as agriculture, on species extinction risk (Polaina et al, 2018), to quantify links between species extinction risk and invasive species (Tingley et al, 2016; Walsh et al, 2012), to characterize the distribution of threatened species (Coll et al, 2015), to predict future biodiversity losses (Andermann et al, 2021; Monroe et al, 2019), and to understand the potential effects of extinction on large-scale diversity patterns (Oliveira et al, 2020; Smiley et al, 2020).…”