Androgenesis: a review through the study of the selfish shellfish Corbicula spp

Abstract

Among the asexual reproductive modes, androgenesis is probably one of the most astonishing and least studied mechanisms. In this 'paternal monopolization', the maternal nuclear genome fails to participate in zygote development and offspring are paternal nuclear clones. Obligate androgenesis is known in only a few organisms, including multiple species of clam in the genus Corbicula. Corbicula is a good system to review the evolutionary consequences of this 'all-male asexuality' because the cytological mechanisms of androgenetic reproduction have been described. In Corbicula, sperm are unreduced and, after fertilization, the maternal nuclear chromosomes are extruded as two polar bodies. Hermaphroditic lineages of Corbicula have a worldwide distribution and seem to reproduce through androgenesis, whereas their sexual relatives have restricted ranges. The invasive success of these androgenetic Corbicula lineages may be linked to their asexual mode of reproduction. We review the phenomenon of androgenesis, focusing on evolutionary perspectives, using the genus Corbicula as an exemplar system.

Figure 1

Schematic representation of the main steps of androgenetic reproduction in Corbicula spp. after fertilization. (1) The maternal chromosomes (in blue) are in metaphase I. The meiotic axis is parallel to the cell cortex. The male pronucleus is indicated in red. (2) The egg is in anaphase I and the maternal chromosomes segregate. (3) The cytoplasm around the asters is distorting and two polar bodies, containing all maternal chromosomes, are formed. (4) The male pronucleus expands. (The male gamete is considered unreduced, here diploid.) (5) Metaphase of the first cleavage (mitosis) of the zygote (with only ‘paternal' chromosomes). (6) Anaphase of first cleavage. (7) Two-cell stage of the zygote. This schematic representation is based on cytological observations in Komaru et al. (1998).

Figure 2

Schematic illustration of mitochondrial genome capture and fixation of mixed cytonuclear genome in the case of the European Corbicula lineages forms R and S (Hedtke and Hillis, 2011; Pigneur et al., 2011b). The ploidy of forms R and S is still uncertain (2n or 3n), but the general mechanism of mitochondrial capture remains the same in the different cases. Here, the egg is considered diploid (unreduced) as it is in metaphase I 15 min after spawning and the reductional division has not occurred yet.

Figure 3

Mitochondrial phylogeny (maximum-likelihood tree) based on a 562 bp fragment of the mitochondrial gene COI from Corbicula spp. (modified from Pigneur et al., 2011b). Bootstrap values for 1000 replications are indicated. Sperm type (mono- or biflagellate) is represented when known. Biflagellate sperm is indicative of androgenesis in Corbicula spp. Invasive lineages are indicated in bold. Origin and GenBank accession numbers of sequences are presented in Table 3. The cytonuclear mismatches (mitochondrial vs nuclear data) represented here are those documented in Lee et al. (2005), Pfenninger et al. (2002), Hedtke et al. (2008) and Pigneur et al. (2011b).

Figure 4

Schematic map showing the current distribution of the main lineages of Corbicula spp. Native and invasive approximate ranges are indicated in black and gray, respectively (modified from McMahon, 1999; Lee et al., 2005). Morphotypes are indicated and corresponding mitochondrial haplotypes (COI) are within parenthesis.