The evolution of diapause in Rivulus (Laimosemion)

Abstract

Annual killifish that are adapted to life in aquatic habitat that dries seasonally have evolved desiccation-resistant eggs capable of undergoing diapause, i.e. developmental arrest, at specific stages during embryology. Although noted for their remarkable ability to live at the land-water interface, species in the genus Rivulus are considered to be nonannual killifish that exhibit typical teleost developmental patterns and no embryonic diapause. Here, we combine a molecular phylogeny with an embryological study in order to demonstrate an independent origin of mid-embryonic diapause within a clade of Rivulus (subgenus Laimosemion) that inhabits small streams or savannah pools. We also observed that some of these species exhibit a short dispersed cell phase separating epiboly and the formation of the embryo axis, which is a feature of development observed only in annual killifish. Lastly, we incubated embryos of Laimosemion species and outgroup taxa in both water and peat moss and observed that on peat moss the embryos of all species are capable of delaying hatching for > 10 days, but when water incubated there are significant differences among species in the duration of this delay before hatching. We hypothesize that the preferred microhabitat of this clade of killifish exposes their embryos to periodic desiccation, creating selection in favour of embryonic diapause.

Prolonged survival out of water is linked to a slow pace of life in a selfing amphibious fish

“…One limitation to our microcosm experiment was that fish were unable to disperse. The natural habitat of mangrove rivulus and other rivuline killifishes typically consists of a mosaic of small, intermittent pools (Turko and Wright, 2015;Furness et al, 2018;Sutton et al, 2018). A high metabolic rate is often correlated with high boldness and activity (e.g.…”

Review of the family Rivulidae (Cyprinodontiformes, Aplocheiloidei) and a molecular and morphological phylogeny of the annual fish genus Austrolebias Costa 1998

“…Monophyly is supported by molecular analyses (Hrbek et al, 2004;Costa 2011aCosta , 2013. This is considered a non-annual genus; however, Furness et al (2018) have found diapause stages in some species similar to those found in annual species, which could represent intermediates steps in the evolution of the annual life cycle.…”

Embryonal life histories: Desiccation plasticity and diapause in the Argentinean pearlfish Austrolebias bellottii

“…Slowing down during early development in nonannuals in response to desiccation might be mostly an immediate response, therefore quiescence, even while there are some lagged effects (however, see Furness et al, ). If genetic assimilation of diapause has occurred in killifish via the evolution of plasticity in response to desiccation, then there has clearly been further plasticity evolution after the emergence of diapause‐like characteristics.…”

“…Their plastic hatching delay showed several characteristics of diapause III which is constitutive in annuals. Since then, Furness, Reznick, Tatarenkov, and Avise () showed that developmental properties presumed to be limited to annuals do occur in some sister taxa. For annual killifish, there are no data allowing a detailed analysis of rates of development and survival during and after a desiccation period.…”