Maternal source of variability in the embryo development of an annual killifish

Abstract

Organisms inhabiting unpredictable environments often evolve diversified reproductive bethedging strategies, expressed as production of multiple offspring phenotypes, thereby avoiding complete reproductive failure. To cope with unpredictable rainfall, African annual killifish from temporary savannah pools lay drought-resistant eggs that vary widely in the duration of embryo development. We examined the sources of variability in the duration of individual embryo development, egg production and fertilization rate in Nothobranchius furzeri. Using a quantitative genetics approach (North Carolina Type II design) we found support for maternal effects rather than polyandrous mating as the primary source of the variability in the duration of embryo development. The number of previously laid eggs appeared to serve as an internal physiological cue initiating a shift from rapid to slow embryo developmental mode. In annual killifish extensive phenotypic variability in progeny traits is adaptive, as the conditions experienced by parents have limited relevance to the offspring generation. In contrast to genetic control, with high phenotypic expression and heritability, maternal control of traits under natural selection prevents standing genetic diversity from potentially detrimental effects of selection in fluctuating environments.

Local variation in embryo development rate in annual fish

“…distribution than others (Geurts & Van den Berg, ; Mazuze, ; Watters, ), any temporary pool still represents an unpredictable ecosystem by its very nature. As parental generations lack any reliable cues on the future environment of their offspring (Furness et al, ; Pinceel et al, ; Polačik et al, ), the environmental stochasticity is accounted for by developmental bet‐hedging in order to avoid reproductive failure (Crean & Marshall, ).…”

“…After the anti‐fungal treatment, 788 eggs were randomly chosen from the pool of fertilized eggs (95–100 per population) and individually incubated in 8 cm 3 compartments of plastic Petri dishes under a 1·5 cm layer of damp peat (Agro CS; http://www.agrocs.cz) (Polačik et al, ). The position of eggs was randomized across different populations.…”

“…Individual embryo development was checked visually during four inspections at 30 day intervals (30, 60, 90 and 120 days‐post‐fertilization; dpf). A focused light source was used to inspect each egg through the bottom of the transparent Petri dish (Polačik et al, ). Where direct observation was compromised by the position of a particular egg ( c .…”

“…Some embryos develop into the pre‐hatching stage in less than 3 weeks, while others may take several years (Cellerino et al, ). Such asynchrony commonly occurs not only at the population level but also within a single clutch incubated under the same conditions (Polačik et al, ). Variation in embryo development allows the fish to cope with a false onset of the rainy season (Wourms, ) when light initial rains are followed by a further period of drought.…”

Changing patterns of growth in a changing planet: How a shift in phenology affects critical life‐history traits in annual fishes

“…Upon resumption of development, embryos may respond to desiccation by entering Diapause II and continue development if the substrate is moistened (Reichard & Polačik, ). There are individual differences in response to external cues (Furness, ; Polačik, Smith, & Reichard, ), resulting in the egg bank comprising embryos at various stages of development. In the studied pools, hatching of the second cohort was possible because the egg banks contained embryos ready to hatch.…”