First empirical evidence of naturally occurring androgenesis in vertebrates

Abstract

Androgenesis among vertebrates is considered a rare phenomenon, with some cases reported so far, but linked to experiments involving gamete manipulation (artificial androgenesis). Herein, we report the first empirical evidence of the natural occurrence of spontaneous androgenesis in a vertebrate, the Squalius alburnoides allopolyploid complex. A genetically screened random sample of a natural population was allowed to reproduce in an isolated pond without any human interference, and the viable offspring obtained was later analysed for paternity. Both nuclear and mitochondrial markers showed that the only allodiploid fish found among all the allotriploid offspring was androgenetically produced by an allodiploid male. This specimen had no female nuclear genomic input, and the sequence of the mitochondrial fragment examined differed from that of the male progenitor, matching one of the parental females available in the pond, probably the mother. The possible role of androgenesis in the reproductive dynamics of this highly successful vertebrate complex is discussed.

Sex chromosomes in meiotic, hemiclonal, clonal and polyploid hybrid vertebrates: along the ‘extended speciation continuum'

“…In particular, most 'asexual' vertebrates exhibit strongly female-biased sex ratios, which is why they have also been referred to as 'unisexual' or 'all-female' species [49,164,192,193]. Such a female bias might result from the simple fact that (hemi-)clonal males cannot generate progeny on their own, since their reproduction requires ova; even in cases like androgenesis [194,195], where clonal sperm replaces egg nuclei from related females. This reliance on eggs could explain why hybrid males are often absent in 'asexual' vertebrate taxa, even if they would be able to produce fertile (hemi-)clonal gametes.…”

Delete and survive: strategies of programmed genetic material elimination in eukaryotes

“…Natural androgenesis is known only in some cypress species ( Cypresses ), bivalves from the genus Corbicula , and occasionally in some fish species and Bacillus stick insects (Mantovani & Scali, 1992 ; Tinti & Scali, 1995 ; Komaru et al ., 1998 ; Komaru, Ookubo & Kiyomoto, 2000 ; Ishibashi et al ., 2003 ; Wang et al ., 2011 b ; Morgado‐Santos et al ., 2017 ). During androgenesis, the maternal genome is eliminated while the paternal genome [or genomes in the case of polyspermy (Mantovani & Scali, 1992 ; Tinti & Scali, 1995 )] continues further development (Komaru et al ., 1998 , 2000 ; Ishibashi et al ., 2003 ) (Fig.…”

Using asexual vertebrates to study genome evolution and animal physiology: Banded (Fundulus diaphanus) x Common Killifish (F. heteroclitus) hybrid lineages as a model system

“…In the following section, we review what is known about Fundulus diaphanus x F. heteroclitus asexual lineages, present some preliminary results from our laboratories, and discuss future research goals. We do not focus extensively on other asexual fishes, so we refer interested readers to reviews by Arai and Fujimoto (2013), Avise (2008, 2012, 2015), Lampert (2009), Lampert and Schartl (2008), Lamatsch and Stöck (2009), and Vrijenhoek (1994), as well as some of the recent research on asexual Poeciliidae (Alberici da Barbiano, Gompert, Aspbury, Gabor, & Nice, 2013; Gabor, Barbiano, & Aspbury, 2013; Schedina, Groth, Schlupp, & Tiedemann, 2018; Schlupp, Riesch, & Tobler, 2007; Stöck, Lampert, Möller, Schlupp, & Schartl, 2010; Warren et al, 2018), Hexagrammidae (e.g., Munehara, Horita, Kimura‐Kawaguchi, & Yamazaki, 2016; Suzuki, Miyake, Arai, & Munehara, 2019), Cyprinidae [ Carassius (Gui & Zhou, 2010; Jiang et al, 2013; Li et al, 2018), Chrosomus (Lafond et al., 2019; Leung & Angers, 2018; Leung et al, 2016, 2018; Mee, 2014; Mee, Brauner, & Taylor, 2011; Mee & Taylor, 2012; Vergilino, Leung, & Angers, 2016), S qualius alburnoides (Collares‐Pereira & Coelho, 2010; Collares‐Pereira, Matos, Morgado‐Santos, & Coelho, 2013; Morgado‐Santos et al., 2017; Pereira, Ráb, & Collares‐Pereira, 2013)], Misgurnus anguillicaudatus (e.g., Kuroda et al., 2018; Kuroda, Fujimoto, Murakami, Yamaha, & Arai, 2019; Kwan, Ko, Jeon, Kim, & Won, 2019; Yamada et al., 2015) and Cobitius spp. (Choleva et al., 2012; Cunha, Doadrio, Abrantes, & Coelho, 2011; Janko et al., 2012, 2018; Ko, Yoon, Kim, & Park, 2015; Majtánová et al., 2016) for further information.…”

“…Engaging in the risky aspects of sex, without any of the proposed benefits, makes the persistence of gynogenesis especially interesting from an ecological and evolutionary perspective (Schlupp, 2005). There is also evidence that at least one vertebrate, the cyprinid Squalius alburnoides, may reproduce by androgenesis (Morgado‐Santos, Carona, Vincente, & Collares‐Pereira, 2017); this form of reproduction results in offspring with only male nuclear, and sometimes mitochondrial chromosomes, so is the “flip‐side of gynogenesis” (reviewed by Lehtonen, Schmidt, Heubel, & Kokko, 2013).…”