Cytonuclear evidence for hybridogenetic reproduction in natural populations of the Australian carp gudgeon (Hypseleotris: Eleotridae)

Abstract

Although most vertebrates reproduce sexually, a small number of fishes, amphibians and reptiles are known in which reproduction is asexual, i.e. without meiotic recombination. In fishes, these so-called unisexual lineages usually comprise only females and utilize co-occurring males of a related sexual species to reproduce via gynogenesis or hybridogenesis. Here, we examine patterns of microsatellite and mitochondrial DNA (mtDNA) variation in a widespread group of freshwater fishes (carp gudgeons; Hypseleotris spp.) to investigate a long-standing proposal that this group includes unisexual forms. We show that the mtDNA genome of most carp gudgeons in tributaries of the Goulburn River belongs to one of two deeply divided clades (∼10% cyt b divergence) and that nuclear variation divides the same individuals into four distinct groups. Group 1 exhibits the genotypic proportions of a random mating population and has a 1:1 sex ratio. Two other groups are extremely sex-biased (98% male, 96% female), exhibit excess heterozygosity at most loci and share at least one allele per locus with group 1. We propose that these two groups represent 'unisexual' hybridogenetic lineages and that both utilize co-occurring group 1 as sexual host. Interestingly, the fourth distinct group appears to represent hybrid offspring of the two putative hybridogenetic lineages. The propagation of clonal haploid genomes by both males and females and the ability of these clones to unite and form sexually mature diploid hybrid offspring may represent a novel mechanism that contributes to the dynamics of coexistence between hybridogenetic lineages and their sexual hosts.

High male incidence and evolutionary implications of triploid form in northeast Asia Carassius auratus complex

“…However, most of unisexual vertebrates, such as kleptogenetic Ambystoma salamanders (Bi and Bogart, 2010;Spolsky et al, 1992), hybridogenetic Poeciliopsis fish (Quattro et al, 1992), gynogenetic Amazon molly (Lampert and Schartl, 2008;Schartl et al, 1995), Phoxinus eosneogaeus hybrids (Angers and Schlosser, 2007), and gynogenetic Cobitis (Janko et al, 2003), have been revealed to have long history and large ranges of geographical distribution (Avise, 2008). And, high genetic diversity has been extensively observed in gynogenetic or hybridogenetic fish (Angers and Schlosser, 2007;Cunha et al, 2011;Schmidt et al, 2011;Stöck et al, 2012), kleptogenetic amphibians (Bi and Bogart, 2010) and parthenogenetic reptiles (Fujita et al, 2007;Kupriyanova, 2009). Significantly, these rare unisexual animals are largely associated with polyploidy origin (Neaves and Baumann, 2011;Otto et al, 2007).…”

Androgenesis: where males hijack eggs to clone themselves

“…One of the lineages consists almost exclusively of males, suggesting some form of asexual reproduction by males [17]. Detailed analyses of genotypes suggest that the male lineage most likely reproduces via hybridogenesis [17,27].…”

“…There are three distinct, co-occurring carp gudgeon lineages in the Murray River in South Australia [17,27]. One of the lineages consists almost exclusively of males, suggesting some form of asexual reproduction by males [17].…”

“…As we explain in the following sections, whether and how diploidization occurs, and under which form of sex determination, greatly affects the predicted fate of androgenetic lineages. While androgenesis is rare in nature, it is 'normal' in some natural populations, including clams of the genus Corbicula [3][4][5], a conifer [6][7][8], a few ants [9][10][11][12] and stick insects [13][14][15][16], and most likely an Australian carp gudgeon [17] (table 1). Androgenesis is also seen sporadically in some species, particularly hymenopterans (ants, bees and wasps), and in some monocots, dicots and gymnosperms (table 1).…”

Improving the ecological understanding of species complexes: the case of piscivory and protracted spawning in the carp gudgeon group Hypseleotris spp. (Eleotridae, Teleostei)

“…Yet, taxonomical difficulties in species identification combined with extensive hybridization (Bertozzi et al, 2000;Schmidt et al, 2011) have resulted in the MDB carp gudgeons to be referred to either as western carp gudgeon (in the broad sense) or as a species complex Hypseleotris spp., otherwise known as 'carp gudgeon group' (Humphries et al, 1999;King et al, 2003;Vilizzi, 2012). Across the MDB, Hypseleotris spp.…”