The role of early life stages in land-invasion and geographic distribution of the semi-terrestrial crabs

This set of studies is the first contribution that helps clarifying the ongoing evolutionary process of terrestrialization of crabs, with relevance to the first life stages, particularly the embryonic phase. Studies on the evolutionary processes and physiology are almost exclusively conducted on adults, often neglecting the first and most vulnerable life stages, such as eggs and larvae. The ontogenesis is not a simple progression toward the complexity of the adult phase, since natural selection operates on all stages of development, independently leading to adaptations that may be partially or totally disconnected from the previous or the following stage. Brachyuran crabs offer an ideal model to study terrestrialization: paleontological and biological evidence corroborates the hypothesis that they are at the dawn of land invasion. The vast majority of terrestrial crabs include species living far from permanent water bodies, but their larvae still need to develop in aquatic media from few days to several days. Embryos therefore represent the link between the terrestrial adult stage and the water dependent larval stage. Brooding mothers and embryos form an ecological unit whose biology is shaped and often driven by the ecological needs of the embryos. As a consequence, an ontogenetic approach, aimed at understanding the eco-physiological traits of embryos during their developmental stages, is fundamental to highlight the adaptive strategies of amphibious carrying mothers and the overall ecological needs of the species. I demonstrate that the egg mass does not suffer from oxygen limitation proofing that the reproductive strategy, and not the level of terrestrialization, affects the dimensions of eggs. Another novel result of my thesis is the experimental verification of the ability of semiterrestrial crabs’ embryos to breath efficiently in air, which is demonstrated by the constant increase of metabolic rate throughout the development. Prolonged exposition to air however poses problems to embryos. A. miersii loses brood and shows massive developmental problems if deprived of water for 18 hours a day. Pachygrapsus marmoratus, after 4 hours of water deprivation, shows a significant increase in concentration of ammonium. The description of the early life history of the two supralittoral species Chiromantes eulimene and Chiromantes ortmanni confirms the strong water dependence of their larvae. As most likely expected from reproduction ecology, embryos of semiterrestrial crabs are half-way adapted between the semiterrestrial adult phase and the aquatic larval one. Since the aquatic-based metabolic pathways are probably maintained, embryos will most likely suffer if exposed to air for prolonged periods. Nevertheless, I suggest that limited aerial exposures of berried mothers are advantageous for mothers and embryos especially during hypoxic events, which are known to occur in shallow coastal waters. Finally, I also show the importance of the first life stages, embryos and larvae, in setting the geographical distribution of two semiterrestrial crabs, Parasesarma catenata and Neosarmatium africanum (= meinerti). The geographical ranges of these two semi-terrestrial crabs are set by the biological bottleneck given by the most vulnerable life stages that, with their narrower thermal windows, limit the geographical expansion of the species range. If this critical role of embryos and larvae is confirmed, research on the physiological tolerance and plasticity of these life stages should be emphasized, to draw realistic scenarios of future species distribution and geographical range shifts due to global warming. Overall, this thesis provides original and fundamental contribution that helps clarifying the evolutionary process of terrestrialization in arthropods in a physiological and ecological contexts, with the general implications for the fitness, persistence and spreading of populations consistently exposed to environmental stress.