SIZE CONSTRAINTS ON THE EVOLUTION OF TERRESTRIAL ANIMAL LINEAGES

Consideration of the constraints on animal terrestrialization often focus on one of two perspectives: the early fossil record (leading to emphasis either on tetrapod vertebrates or on scorpion and trigonotarbid arachnids along with millipedes) or modern transitions (leading to emphasis most likely on crustaceans or gastropods). However, these approaches are biased towards the large. Alternatively, focus might be on the physiological constraints themselves and consideration of the body sizes that might minimize them. Minimum body dimensions of modern terrestrial animals span at least six orders of magnitude from more than a meter down to less than ten microns. Much of that range is confined to the diminutive soil fauna with minimal potential for fossil preservation, but it is these smaller sizes that avoid key constraints on terrestrialization. For example, respiration is radically different in or out of water, but land animals less than about a mm wide can simply exist without specialized respiratory structures. Although not always fully resolved, phylogenetic topologies within the major land arthropod lineages—arachnids, myriapods, hexapods—are consistent with such small sizes being ancestral for each lineage as a whole. However, each is unlikely to have been dramatically smaller, since body widths approaching 100 microns or less are associated both with eutelic development and with the loss of circulatory system, complex eyes, and body cavity.

With this size window in mind, it is remarkable how much of the modern soil fauna was already present by the Devonian. Overall, origins of terrestrial animal lineages prior to the Carboniferous appear to have had ancestral body widths of a mm or less: arachnids, myriapods, hexapods, tardigrades, various nematodes. All terrestrial lineages that were ancestrally large—tetrapods, onychophorans, earthworms, leeches, isopods, nemerteans, various decapods and snails—originated in the complex ecosystems of the Carboniferous and later times that would have provided more opportunity to moderate some of the challenges of terrestrial life at larger sizes. Later originations could also be small—e.g. enchytraeid annelids, rotifers, planarians, amphipods—but early originations were only small. These patterns have important implications for the early evolution of terrestrial ecology.