Reproduction in cold water: paradigm changes in the 20th century and a role for cidaroid sea urchins

Abstract At the beginning of the 20th century, powerful ideas about the biology of marine animals in cold waters (polar and deep sea) were in early stages of development. (1) General similarities between some Arctic and Antarctic species suggested a past or present continuity between the poles, possibly through tropical submergence. (2) The discovery of subantarctic species brooding their offspring suggested that supposedly harsh polar conditions select against species with pelagic, dispersive larvae. (3) The linkage between seasonal temperature changes and seasonal reproduction suggested that where temperatures were constant, as in polar and deep seas, reproduction would be aseasonal or continuous throughout the year. (4) Recognition of the phenomenon of metabolic temperature adaptation suggested that animals living in cold water should exhibit rates of physiological processes similar to rates in warmer environments. Observations and experiments throughout the first half of the 20th century generally supported and reinforced these ideas. During the second half of the 20th century, however, the generality of these paradigms broke down. Detailed analyses of fuller data indicated that Arctic, Antarctic, and deep-sea faunas are not the same and probably have different phylogenies reflecting different vicariant histories. Moreover, many species in these habitats have pelagic larvae, they generally spawn seasonally, and their physiological processes (respiration, gametogenesis, development, feeding, growth) are slow, showing little evidence of the expected temperature adaptation. Nevertheless, entering the 21st century, we are challenged by important exceptions that do support many of the earlier ideas. Bipolarity in some groups does indicate relict distributions, and other groups show equatorial submergence. Moreover, major species-rich clades in the Antarctic (unlike the Arctic) do brood their young. Most species with pelagic larvae produce non-feeding (lecithotrophic) larvae rather than feeding (planktotrophic) larvae, and these, along with brooding species, generally do reproduce throughout the year. Yet brooding is almost certainly not an adaptation to low temperatures and low larval food supply, as supposed earlier; instead, the species-rich clades of brooders probably reflect enhanced speciation under unique conditions in the Antarctic. In addition, despite recent evidence of constraints on metabolic flexibility, low metabolic rates may themselves be adaptations to Antarctic conditions. Just as a growing body of “exceptions” to the early 20th century paradigms led to their breakdown, these persisting exceptions to current ideas demand that our existing paradigms be re-examined for further insight into the biology of marine animals in cold water. Cidaroid echinoids, in particular, appear to support some of the earlier ideas. The group consists of one or possibly two clades that make up over 80% of the species of regular sea urchins in the Antarctic; several species extend into the deep sea. One putative species is nearly bipolar, extending from the Antarctic shelf into the deep sea and then north in the eastern Pacific to Alaska. All the species appear to brood embryos, but development in the brood might be facultative. Reproduction seems to be aseasonal, albeit infrequent. Growth rates are probably very slow and longevity very long. Current work begun with ANDEEP is directed at resolving the phylogenetic history of this group to better understand unusual reproductive and other features in cold-water marine animals.