The Colonization of Land by Crustaceans

Pomona College, Claremont CA

Investigators

Abstract

Although several groups of animals have colonized land, the evolutionary changes that have made this possible are only superficially understood. This is due in large part to difficulties in resolving the evolutionary relationships among terrestrial taxa within a particular group, and their relationships to aquatic counterparts, problems that leave the status of both the aquatic ancestors and transitional or 'prototypal' terrestrial species unresolved. In the case of the three most successful terrestrial taxa, the tetrapod vertebrates, the insects, and the arachnids, it is clear that living descendents of these ancestral groups no longer survive. This greatly limits our understanding of the adaptive transitions that have made terrestrial life possible. Terrestrial isopods, commonly known as woodlice or sowbugs, provide possibly the best 'model system' for studying the evolution of physiological systems accompanying the aquatic-terrestrial transition. In contrast to the other major terrestrial animals, they are represented by living groups that occupy diverse habitats from marine aquatic to 'transitional' intertidal and fully terrestrial. The evolutionary relationships of living species have recently been elucidated in considerable detail from comparative anatomy and molecular phylogenetic techniques, and these indicate that the aquatic and intertidal species are more basal, and thereby more closely related to other marine isopods, than the more 'derived' terrestrial species. Furthermore, they indicate at least three independent origins of a terrestrial habit. Taken together, these factors provide an excellent basis for comparative physiological studies. By reconstructing an evolutionary lineage from marine to fully terrestrial, and comparing specific physiological traits across species taken from that lineage, it is possible to understand the physiological transitions involved. Building a picture of the physiological changes in this way allows us not only to study specific changes that have accompanied terrestriality, but also to compare adaptive solutions among the independent terrestrial radiations. Studies will focus on five main physiological systems. Water vapor absorption (WVA) is known from only one group of terrestrial isopods and allows animals to recover water in ambient humidities exceeding approximately 87%. The condensation of water vapor involves the secretion of concentrated salt solution by the gills to generate reduced vapor pressure. A key question in explaining the evolution of WVA is to unravel the ancestral functions of salt secretion in intertidal or terrestrial species. Like WVA, both nitrogenous excretion and ion regulation are closely associated with water balance. Terrestrial isopods excrete nitrogenous waste as ammonia gas, and this presents an intriguing solution to water conservation by potentially eliminating simultaneous water losses. Ammonia volatilization does, however, cause acidification of the gill surface and buffering of accumulated acid is essential for the process to work. Understanding the buffering mechanism, and its possible preadaptive functions, is thus essential in explaining how ammonia volatilization evolved. Most terrestrial animals possess efficient mechanisms for regulating blood solute concentration, protecting the tissues against osmotic hydration or dehydration and resultant changes in cell volume. Aquatic isopods are capable of regulating blood salt concentration in both elevated (hyper-osmotic) and depressed (hypo-osmotic) external salinities. Recent studies have shown that intertidal species counteract increasing blood salinities imposed by dehydration by excreting salts across the gills, as in aquatic species. Fully terrestrial species cannot excrete salts, however, since dietary salts are impoverished. One group has been shown to down-regulate blood salts by sequestration in the hindgut during dehydration. Although regulation has been demonstrated in other groups, the mechanisms await investigation. At least one group appears to have lost the ancestral capacity for osmoregulation. As well as osmotic concentration imposed by dehydration, isopods may face osmotic dilution during rain showers, a danger exacerbated by their permeable cuticles. The mechanisms by which excess water is eliminated are essentially unstudied, though recent work indicates a role of the maxillary glands in producing dilute urine. The remaining areas of study will focus on reproductive physiology, specifically maternal regulation of the embryonic environment and ion regulation of periembryonic fluid by the eggs. The eggs and newly hatched juveniles (mancas) are brooded in a fluid-filled marsupium. Marine isopods flush this with seawater, but terrestrial species either fill it from external water sources or from the blood. Desiccation and thermal stresses on land demand either maternal regulation of the marsupial environment or high physiological tolerance in early developmental stages. Recent studies have shown extreme tolerance of osmolality, pH, temperature and ammonia extremes in embryos of terrestrial isopods, and pH and ion regulation appears to employ a greatly enlarged embryonic 'dorsal organ'. Studies will investigate ion transport mechanisms in this organ. Comparisons within lineages will reveal whether the enlargement of the dorsal organ is a unique terrestrial innovation and will test the hypothesis that its ancestral function was calcium uptake for mineralization of the cuticle.