Allometry reveals trade-offs between Bergmann’s and Allen’s rules, and different avian adaptive strategies for thermoregulation

Allometry reveals trade-offs between Bergmann’s and Allen’s rules, and different avian adaptive strategies for thermoregulation

Why animals evolved such a huge diversity of body forms is a question that for long bothered biologists. Of course, an animal’s body size and shape always go in tandem with ecological functionality, e.g. tallness in giraffe that allows browsing tree canopies in savanna, small size in rodents that allows fitting many burrows, long beaks in hummingbirds that allows accessing nectar from the tube-shape flowers, long legs in flamingos that allows exploring shallow water while keeping the body dry. However, the evolution of body size and shape was not unlimited, but met significant constraints, i.e. due to thermoregulation, as described by Bergmann’s and Allen’s rules. Bergmann’s rule states that being larger allows to effectively conserve the warmth and thus is favored in cold climates, while being smaller facilitates temperature exchange and thus benefits in warm climates. Allen’s rule states that short appendages (e.g. legs or beaks) allow saving more heat and thus are advantageous in cold conditions, while long appendages ensure efficient temperature exchange, so they are efficient in hot conditions.

Modern advances in ecology provide evidence that Bergmann’s and Allen’s rules apply to many animal clades, especially birds and mammals (including human). These ecogeographic rules are valid both when comparing species to species and when comparing individuals of the same species. The differences in body size and shape are evident when looking at temporary trends in body size and shape, as climate change necessitates these animals to adapt to novel thermal environments. Bergmann’s and Allen’s rules are more evident when comparing animal communities from different regions, as those also evolved under the pressure of thermoregulation. For example, mooses, penguins or capercaillies are larger than their closest relatives from hotter climates, while hummingbirds, toucans, hornbills, flamingos or giraffes have larger appendages (beaks or legs) than their closest relatives from colder climates. However, many animal species constitute counter-examples of Bergmann’s and Allen’s rules, which led to questioning of the generality of these ecogeographic patterns. Why do the largest terrestrial animals on Earth, e.g. elephants, giraffes, gorillas, ostriches or rea, occur in hot instead of cold climates? How can animals with very long appendages, such as reindeers, hares, albatrosses or swans, survive in so cold climates? Here we provided an explanation for these phenomena.

the common ostrich Struthio camelus (Leszek Noga), the jabiru Jabiru mycteria (Jacek Betleja), the rufous-tailed hummingbird Amazilia tzacatl (Damian Kurlej), the great hornbill Buceros bicornis (Paweł Czechowski)
Examples of birds from hot climates: the common ostrich Struthio camelus (Leszek Noga), the jabiru Jabiru mycteria (Jacek Betleja), the rufous-tailed hummingbird Amazilia tzacatl (Damian Kurlej), the great hornbill Buceros bicornis (Paweł Czechowski)

In this study, we coupled the global variation in avian body mass, beak and leg length with environmental temperature assessed across geographic ranges of 9962 bird species (99.7% of all world’s species) to simultaneously examine Bergmann’s and Allen’s rules. Our results reveal the trade-off between the two rules. In other words, animals have two ways to adapt to novel climates – first through the shift in body size, and second through changes in the size of appendages. The occurrence of giant birds in hot climates is enabled by their long legs (e.g. ostriches, rea) or beaks (e.g. jabiru), which play in these species as thermoregulatory organs. While some species with fairly large beaks (e.g. swans), or large legs (e.g. herons), can survive in surprisingly harsh conditions because of larger body sizes, as large size ensures good temperature savings. Our study finds that the larger is the body, the larger beak is required to settle in hot climates, while the longer is the beak, the larger body is allowed to thrive in hot temperatures. Similarly, the larger the body, the larger legs are required to settle in warm conditions, while the longer the legs, the larger body is allowed to reside in warm conditions. Surprisingly, we find evolutionary pressure for reducing leg length toward hotter climates (inverse of Allen’s rule), presumably for functional reasons. However, the reduction of legs in hot climates is possible in smaller birds (e.g. hummingbirds or passerines), which do not acquire high heat loads. Therefore, our study explains that we should not expect both Bergmann’s and Allen’s rules to operate simultaneously. Instead, either shifts in size or shape have been occurring throughout evolutionary history of animals. Alternatively, both rules operated, but to a lesser extent, such as in capercaillies or penguins, which can reside in harshest climates of the world thanks to average-sized and compact bodies.

whooper swan Cygnus cygnus (Grzegorz Sobczak) , grey heron Ardea cinerea (Andrzej Kośmicki), Adélie penguin Pygoscelis adeliae (Jacek Betleja), western capercaillie Tetrao urogallus (Dariusz Żelasko)
Examples of birds from cold climates: the whooper swan Cygnus cygnus (Grzegorz Sobczak), the grey heron Ardea cinerea (Andrzej Kośmicki), the Adélie penguin Pygoscelis adeliae (Jacek Betleja), the western capercaillie Tetrao urogallus (Dariusz Żelasko)

We also found that in larger birds, the summarized size of beak and tarsus is important for thermoregulation, i.e. larger species from hot climates may evolve either larger beaks or larger legs (or both, but to a lesser extent). However, the trade-off in the evolution of these two types of appendages does not apply to smaller birds, in which the size of the beak and legs are correlated, possibly for functional or physiological reasons. The compromise between avian body size, beak length and leg lengths explains only up to 20% of the variation in avian thermal environment, underlining that birds involve many other mechanisms to cope with thermoregulation, i.e. variation in behavior, coloration or feather structure. Our results should be thus seen only as tendencies, a part of a more complicated story that waits for further studies. Moreover, these patterns rather do not apply when comparing unrelated lineages (e.g. penguins with ostriches or hummingbirds with storks), but they are rather more robust across closely-related species.

We conclude that shifts in body size and shape may have been intertwined through the evolutionary history of animals when they adapted to thermal environments. The evolution of body form possibly wants to trick ecogeographical rules to evolve functional traits. This explanation highlights the diverse mechanisms that animals may involve to expand across the diverse environments on Earth. Furthermore, as we experience the global increase in temperatures, we should expect mainly large animals to evolve more complicated shapes (e.g. elongate in appendages), while mainly compact-bodied animals to shrink in size.

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