The water-to-land transition stands as one of the most significant events in vertebrate evolution, giving rise to the two major groups of living land vertebrates—amniotes and lissamphibians—which occupy markedly different ecological niches.
While lissamphibians are diverse today, they are limited to small body sizes, ranging from 0.03 to 10,800 grams. This limitation may stem from constraints imposed by their respiratory system, characterized by cutaneous gas exchange and buccal pumping (i.e., using the mouth cavity) for lung ventilation. These respiratory modes are efficient in water but less so in air, due to the slower excretion of waste carbon dioxide (CO2). This favors small body sizes, which maximize the surface area-to-volume ratio critical for effective cutaneous gas exchange.
In contrast, amniotes display disparate body sizes—ranging from 0.2 to 180,000,000 grams among living species—and exhibit a broad dietary range. This has made them the dominant group in terrestrial ecosystems since the Early Permian, approximately 299 million years ago. Amniotes ventilate their lungs via rib motions, a process known as costal lung ventilation. This mechanism enables high-volume lung ventilation and efficient CO2 excretion on land, allowing amniotes to overcome the evolutionary constraints that limit the maximum body size attainable by terrestrial vertebrates.
Key hypotheses of vertebrate terrestrialization propose a plausible link between body size evolution and the advent of costal lung ventilation during the deep divergence between amniote and lissamphibian antecedents. However, this long-standing hypothesis remained incompletely tested until recently.
To address this gap, a research team from the Institute of Vertebrate Paleontology and Paleoanthropology (IVPP) of the Chinese Academy of Sciences evaluated the evolution of body size, skull shape, and respiratory traits using a novel dataset of 344 fossil species. The study focused on early-diverging land vertebrates from the Middle Devonian to the Early Permian.
Their findings were published in Science Advances on April 1.
The team's analyses confirm that different lineages of early land vertebrates exhibited distinct patterns of body size evolution. Both amniote and lissamphibian ancestors independently shifted into small-bodied adaptive zones from a large-bodied common ancestor. Notably, lissamphibian precursors showed stronger constraints on body size evolution. In contrast, amniote-lineage land vertebrates experienced a relaxation of these constraints, enabling them to expand their maximum body size limit over the course of their evolutionary history.
Additionally, the study verifies that buccal lung ventilation was the ancestral respiratory mode of all land vertebrates, which was inherited by lissamphibian precursors. Traits associated with costal lung ventilation subsequently evolved in the lineage leading to modern amniotes. For example, ribs curved along the mesiodistal axis and an elongated cervical region emerged early in stem amniotes, suggesting that these ancestors of modern reptiles and mammals already used costal lung ventilation.
The retention of buccal lung ventilation in lissamphibian ancestors led to an increased reliance on cutaneous CO2 excretion. This aligns with the strong constraints that favor small body sizes in this group—smaller bodies maximize the surface area-to-volume ratio necessary for efficient cutaneous gas exchange—and this trait has been passed down to modern lissamphibians.
The evolution of costal lung ventilation in amniote-lineage land vertebrates not only relaxed body size constraints but also freed skull shape from the functional limitations imposed by buccal lung ventilation. Amniotes evolved deeper skulls, which enabled the functional partitioning of adductor muscles. This adaptation enhanced their ability to exert static pressure during tooth occlusion, a key prerequisite for the evolution of herbivory. This innovation allowed amniotes to occupy new ecological niches by digesting plant resources, with multiple lineages of both herbivores and their predators overcoming constraints on maximum body size during the Early Permian.
Today, amniotes exhibit even greater disparity in body size among terrestrially adapted species, ranging from gigantic multi-ton mammalian herbivores to dwarfed lizards weighing only a few grams. In contrast, lissamphibians remain restricted to small sizes due to their reliance on cutaneous CO2 excretion.
This study provides convincing evidence that these markedly different biological traits in living members of both groups diverged shortly after their origin, establishing the foundation for modern terrestrial ecosystems hundreds of millions of years before the extensive radiation of extant species.
