Date Published: March 24, 2018
Publisher: John Wiley and Sons Inc.
Author(s): Chi‐Kuo Hu, Anne Brunet.
The African turquoise killifish has recently gained significant traction as a new research organism in the aging field. Our understanding of aging has strongly benefited from canonical research organisms—yeast, C. elegans, Drosophila, zebrafish, and mice. Many characteristics that are essential to understand aging—for example, the adaptive immune system or the hypothalamo‐pituitary axis—are only present in vertebrates (zebrafish and mice). However, zebrafish and mice live more than 3 years and their relatively long lifespans are not compatible with high‐throughput studies. Therefore, the turquoise killifish, a vertebrate with a naturally compressed lifespan of only 4–6 months, fills an essential gap to understand aging. With a recently developed genomic and genetic toolkit, the turquoise killifish not only provides practical advantages for lifespan and longitudinal experiments, but also allows more systematic characterizations of the interplay between genetics and environment during vertebrate aging. Interestingly, the turquoise killifish can also enter a long‐term dormant state during development called diapause. Killifish embryos in diapause already have some organs and tissues, and they can last in this state for years, exhibiting exceptional resistance to stress and to damages due to the passage of time. Understanding the diapause state could give new insights into strategies to prevent the damage caused by aging and to better preserve organs, tissues, and cells. Thus, the African turquoise killifish brings two interesting aspects to the aging field—a compressed lifespan and a long‐term resistant diapause state, both of which should spark new discoveries in the field.
Aging is one of the greatest risk factors for many diseases, and it ultimately restricts the lifespan of organisms by increasing the probability of death (Dillin, Gottschling & Nystrom, 2014; Guarente, Ruvkun & Amasino, 1998; Kennedy et al., 2014; Kenyon, 2005; Niccoli & Partridge, 2012). Since the discovery and characterization of the first long‐lived mutants in Caenorhabditis elegans and Saccharomyces cerevisiae more than two decades ago (Kaeberlein, McVey & Guarente, 1999; Kenyon, Chang, Gensch, Rudner & Tabtiang, 1993; Morris, Tissenbaum & Ruvkun, 1996; Ogg et al., 1997; Wang et al., 1993), the concept that aging is a malleable biological process has been well embraced (Finch & Ruvkun, 2001; Gems & Partridge, 2013; Kennedy, 2008; Kenyon, 2005, 2010).
First collected and identified as a new species in 1969, the African turquoise killifish is native to East Africa, where it is found exclusively in Zimbabwe and Mozambique (Furzer, 1969; Jubb, 1971; Parle, 1970). While its short‐lived nature was broadly known among killifish hobbyists, the turquoise killifish remained unnoticed to the research community for decades. That was until 2003, when Alessandro Cellerino’s group at the Scuola Normale Superiore, in Pisa, Italy, first proposed to use it as a research organism for aging and published its first lifespan of ~2 months (Valdesalici & Cellerino, 2003). Since then, the increased knowledge and improved husbandry have significantly lowered the early mortality rate in captivity. The median lifespan has been thus gradually extended and eventually stabilized at around 4–6 months (Figure 1), with similar numbers reported by multiple institutes across North America and Europe (Polacik et al., 2016; Reichwald et al., 2015; Valenzano et al., 2015).
The turquoise killifish is also particularly interesting in that it has two distinct phases with opposing features: (i) a naturally compressed lifespan, with rapid development, sexual maturation, and aging; and (ii) a diapause state, which is a long‐lived form of resistance to a variety of stresses and to damages due to the passage of time. These unique features are evolutionary adaptation to its extreme habitat (Blazek, Polacik & Reichard, 2013). The turquoise killifish naturally live in ephemeral ponds in Mozambique and Zimbabwe where water is only present during the brief rainy season. The rainy season is followed by a prolonged dry season, during which the ponds entirely dry up (Bartakova et al., 2013; Furzer, 1969; Jubb, 1969, 1971; Reichard et al., 2009). This extreme habitat challenges the inhabiting species not only to propagate fast within the short rainy season, but also to survive through the following long dry season. The turquoise killifish has adapted, overevolutionary times, to this extreme environment by having a life history composed of two distinct phases—a fast‐growing (and fast‐aging) phase in the rainy season and then a suspended (and long‐lived) phase in the dry season (Bartakova et al., 2013; Blazek et al., 2013; Reichard et al., 2009; Figure 4). Importantly, these two phases remain unchanged in captivity, even in constant water (Polacik et al., 2016), indicating that both are under genetic determination.
As highlighted in this review, the turquoise killifish has emerged as a promising new research organism for vertebrate aging and aging‐related diseases. With its unique features—a naturally compressed lifespan and a suspended developmental state—the turquoise killifish nicely complements the currently used research organisms for a more systematic understanding of aging and longevity.
Both authors declare to have no conflict of interest.