How maternal age and environmental cues influence embryonic developmental pathways and diapause dynamics in a North American annual killifish.

Temporary pools are variable environments with seasonal drought/flood phases. Annual killifish have adapted to life in temporary pools by producing embryos that undergo diapause to traverse the dry phase. To fill existing knowledge gaps about embryo diapause regulation and evolution in annual killifishes, we test the effect of maternal age, incubation temperature, and incubation medium on diapause induction and length in Millerichthys robustus, the only North American fish species that has evolved an annual life history. All embryos at extreme temperatures follow a defined developmental pathway: skipping diapause at 30°C, and entering diapause at 18°C, both regardless of maternal age, and incubation medium. However, maternal age, and incubation medium influenced whether diapause is entered, and time arrested in diapause for embryos incubated at 25°C. At 25°C, five-week-old, and 52-week-old females produced more embryos that entered diapause than 26-week-old females. Also, embryos incubated in aqueous medium skipped diapause more frequently at this intermediate temperature. Millerichthys developmental dynamics associated with maternal age under intermediate range of temperatures are likely adapted to the particular patterns of flood/drought in North American temporary pools. Millerichthys also exhibits developmental patterns largely comparable with other annual fishes, probably due to common seasonal patterns in temporary pools.

Omar DC ，Sharon VC ，Alejandra MB ，M Muñoz-Campos T ... -  《-》

Developmental ecology of annual killifish Millerichthys robustus (Cyprinodontiformes: Cynolebiidae).

Populations of annual killifishes persist in temporary water bodies over the dry season through the expression of diapause in their drought-resistant embryos. Environmental cues may influence expression of the diapause phenotype during embryonic incubation. Millerichthys robustus is the only annual killifish distributed in North America. The aim of this review is to analyze the ecology of M. robustus development and contrast this with that of annual killifishes in austral locations. The temporary water bodies inhabited by M. robustus present the following environmental conditions: flood, drought, and humidity. During the flooding period, the environment presents the lowest temperatures, shortest photoperiod, and highest precipitation, and embryos were found in diapause I. The drought period features the highest temperatures and lowest precipitation, and embryos were found in diapause II. In contrast, during the humid period at the beginning of the rainy season, embryos were found in diapause I, II, and III, associated with the longer photoperiod and high temperatures. These dynamics of the diapause phenotypes can be explained by a combination of the strategies of phenotypic plasticity during flood and drought periods, and bet-hedging during the humid period. Moreover, the microenvironmental conditions in which embryos were buried could influence developmental trajectories. Developmental Dynamics 246:802-806, 2017. © 2017 Wiley Periodicals, Inc.

Domínguez-Castanedo O ，Valdesalici S ，Rosales-Torres AM 《-》

The evolution of an annual life cycle in killifish: adaptation to ephemeral aquatic environments through embryonic diapause.

An annual life cycle is characterized by growth, maturity, and reproduction condensed into a single, short season favourable to development, with production of embryos (seeds, cysts, or eggs) capable of surviving harsh conditions which juveniles or adults cannot tolerate. More typically associated with plants in desert environments, or temperate-zone insects exposed to freezing winters, the evolution of an annual life cycle in vertebrates is fairly novel. Killifish, small sexually dimorphic fishes in the Order Cyprinodontiformes, have adapted to seasonally ephemeral water bodies across much of Africa and South America through the independent evolution of an annual life history. These annual killifish produce hardy desiccation-resistant eggs that undergo diapause (developmental arrest) and remain buried in the soil for long periods when fish have perished due to the drying of their habitat. Killifish are found in aquatic habitats that span a continuum from permanent and stable to seasonal and variable, thus providing a useful system in which to piece together the evolutionary history of this life cycle using natural comparative variation. I first review adaptations for life in ephemeral aquatic environments in killifish, with particular emphasis on the evolution of embryonic diapause. I then bring together available evidence from a variety of approaches and provide a scenario for how this annual life cycle evolved. There are a number of features within Aplocheiloidei killifish including their inhabitation of marginal or edge aquatic habitat, their small size and rapid attainment of maturity, and egg properties that make them particularly well suited to the colonization of ephemeral waters.

Furness AI 《-》

The complete genome sequence of the protogynous hermaphrodite North American annual killifish Millerichthys robustus (Rivulidae, Cyprinodontiformes).

Domínguez-Castanedo O ，Berbel-Filho WM ，Pirro S ，Valdez-Carbajal S ... -  《-》

Convergent evolution of alternative developmental trajectories associated with diapause in African and South American killifish.

Annual killifish adapted to life in seasonally ephemeral water-bodies exhibit desiccation resistant eggs that can undergo diapause, a period of developmental arrest, enabling them to traverse the otherwise inhospitable dry season. Environmental cues that potentially indicate the season can govern whether eggs enter a stage of diapause mid-way through development or skip this diapause and instead undergo direct development. We report, based on construction of a supermatrix phylogenetic tree of the order Cyprinodontiformes and a battery of comparative analyses, that the ability to produce diapause eggs evolved independently at least six times within African and South American killifish. We then show in species representative of these lineages that embryos entering diapause display significant reduction in development of the cranial region and circulatory system relative to direct-developing embryos. This divergence along alternative developmental pathways begins mid-way through development, well before diapause is entered, during a period of purported maximum developmental constraint (the phylotypic period). Finally, we show that entering diapause is accompanied by a dramatic reduction in metabolic rate and concomitant increase in long-term embryo survival. Morphological divergence during the phylotypic period thus allows embryos undergoing diapause to conserve energy by shunting resources away from energetically costly organs thereby increasing survival chances in an environment that necessitates remaining dormant, buried in the soil and surrounded by an eggshell for much of the year. Our results indicate that adaptation to seasonal aquatic environments in annual killifish imposes strong selection during the embryo stage leading to marked diversification during this otherwise conserved period of vertebrate development.

Furness AI ，Reznick DN ，Springer MS ，Meredith RW ... -  《-》