Reproductive biology of annual killifishes and its relationship with embryonic survival during diapause: Millerichthys robustus (Cyprinodontiformes: Cynolebiidae) as an integrative model

Diapause is a metabolic arrest expressed by annual killifish embryos as an extreme adaptation to persist in environments that show alternate periods of favourable-hostile conditions along the annual cycle. Survival under deteriorated condition can be considered as the final consequence of a previous set of complementary morphophysiological and behavioral processes in adult fishes. Millerichthys robustus is the only annual fish that has developed an annual life history in North America wherewith allow us to consider it as an emerging model for annual killifishes to review, analyze and integrate the knowledge about its reproductive biology involved in allowing the embryos in diapause to survive face the hostile environmental condition. First, we review developmental ecology of Millerichthys embryos throughout different periods (flood, drought and humid) of the annual life cycle showing the possible developmental trajectories in situ. We then analyze: (i) the way in which embryos achieve survive drought from protective cortical structures (perivitelline space and egg envelope) that present dynamic changes according to the conditions to which they are exposed buffering the harmful effects of high temperatures and water loss. (ii) The nature and origin of these protective structures during the ovogenesis (cortical alveoli and zona pellucida give rise to the perivitelline space and egg envelope respectively and oil droplets represent an emergency nutritional reserve). (iii) Sexual synchronization through secretion of pheromones and the reproductive behavior that allows them to spawn under the substrate. Embryonic survival is achieved by success of simplest interactions between reproductive biology elements prior to embryo development.