Androdioecy in Kryptolebias killifish and the evolution of self-fertilizing hermaphroditism

Abstract

Kryptolebias marmoratus is an important experimental fish, and is considered to represent the only vertebrate species comprising self-fertilizing hermaphroditic individuals. Subsequent to the discovery of this unusual mode of reproduction, approximately 50 years ago, K. marmoratus has been the focus of a series of studies. However, little is known about the evolution of this rare reproduction mode, and data on the biology of closely related species are still unavailable. The present study aimed to histologically analyse the gonads of three K. marmoratus congeners (i.e. Kryptolebias ocellatus, Kryptolebias caudomarginatus, and Kryptolebias brasiliensis) to check the distribution of features related to hermaphroditism that are useful for forming hypotheses about the origin and evolution of the self-fertilization mode of reproduction through the available phylogenies. The data obtained demonstrate that populations of K. caudomarginatus consist of males and hermaphrodites, which supports the hypothesis that hermaphroditism arose at the base of the clade containing K. caudomarginatus, K. marmoratus, and K. ocellatus as a first step towards a more advanced condition, uniquely shared by both K. marmoratus and K. ocellatus, in which males are rare or absent in natural populations, with the subsequent occurrence of self-fertilization.

First record of a male of Kryptolebias hermaphroditus Costa, 2011 (Cyprinodontiformes: Cynolebiidae)

“…While researchers have addressed some aspects of systematics (Costa, 2006(Costa, , 2011, evolutionary history (Costa et al, 2010;Tatarenkov et al, 2009Tatarenkov et al, , 2011, and geographic distribution (Sarmento-Soares et al, 2014;Lira et al, 2015), there is little available information regarding natural history, ecology and population dynamics. Despite the large gap in our knowledge of the biology of K. hermaphroditus, the recent studies above mentioned, including the present one, suggest some interesting perspectives for studies on evolution, morphology, behavior and physiology across the species' wide geographic distribution in the mangroves of the Brazilian coast.…”

“…Although the overall taxonomy of Kryptolebias Costa, 2004 is confusing (Costa, 2006), the K. marmoratus species group is well supported by both molecular (Tartarenkov et al, 2009) and morphological data (Costa et al, 2010). The species comprising this group, K. marmoratus (Poey, 1880), K. ocellatus (Hensel, 1868) and K. hermaphroditus Costa, 2011, inhabit estuarine areas associated with mangroves, ranging from southeastern United States of America to southern Brazil (Costa, 2011).…”

“…The species comprising this group, K. marmoratus (Poey, 1880), K. ocellatus (Hensel, 1868) and K. hermaphroditus Costa, 2011, inhabit estuarine areas associated with mangroves, ranging from southeastern United States of America to southern Brazil (Costa, 2011). Besides this unusual brackish habitat, these species are also unique among aplocheiloid killifishes due to the absence of females, which are replaced by hermaphrodites (Costa et al, 2010).…”

“…This clade represents the only occurrence of self-fertilizing hermaphroditism among vertebrates (Tartarenkov et al, 2009;Costa et al, 2010). Because of its reproductive mixedmated system, K. marmoratus has been a popular model species for embryological, physiological, behavioral and genetic studies (Avise & Tatarenkov, 2015).…”

Allard's argument versus Baker's contention for the adaptive significance of selfing in a hermaphroditic fish

“…The Mangrove Rivulus belongs to a small killifish clade that includes several closely related taxa with proclivities for hermaphroditism and in some cases self-fertilization (27,28). Selfing by Kmar was discovered in the early 1960s (29), and in nature it yields highly homozygous lines composed of individuals so genetically uniform as to be, in effect, clonally identical to one another (30).…”