Allelic inheritance in naturally occurring parthenogenetic offspring of the gonochoric sea star Patiria miniata

In laboratory studies of fertilization using the gonochoric broadcast-spawning asterinid sea star Patiria miniata, we found many cases in which some mature eggs spawned by females formed cleavage-stage embryos and feeding bipinnaria larvae without fertilization by sperm. Segregation of maternal microsatellite alleles among the parthenogenetic offspring of known heterozygous females was consistent with several specific modes of asexual reproduction, including polar body suppression. Cryptic outcrossing by sperm contamination was ruled out by the failure to observe non-maternal alleles. The potential for asexual reproduction by the normally outcrossing members of P. miniata may suggest a shared propensity for asexuality among asterinid species from several clades in which isolated adults can produce offspring without outcrossing. Additional key words: 1-methyladenine, automixis, thelytoky, mating systems Asterinid sea stars have highly diverse modes of spawning, fertilization, and larval development (Byrne 2006). Adults of several genera (including Meridiastra, Patiria, and Patiriella) are large, gonochoric broadcast spawners with planktonic outcrossing fertilization. In contrast, adults of some Asterina, Cryptasterina, and Parvulastra species are capable of reproduction in isolation. The broad phylogenetic distribution of this capability among asterinid lineages (Keever & Hart 2008) suggests a general predisposition toward non-outcrossing reproduction among members of this family (Byrne 2006). All asterinids that are capable of reproducing without a mate are small bodied simultaneous hermaphrodites (e.g., Byrne 1996) that produce very small amounts of sperm and have been assumed to selffertilize (Byrne et al. 2003). However, parthenogenesis is a potential alternative mode of reproduction for these and other species (Watts et al. 2006; de Meeûs et al. 2007). Examples of natural parthenogenesis (e.g., Yamaguchi & Lucas 1984) are rare among echinoderms, but artificial induction of parthenogenesis in gonochoric outcrossing sea stars has been widely used in studies of cell cycle control, intracellular signalling, and egg activation (e.g., Hamaguchi 2001; Sasaki & Chiba 2004; Mita 2005; Mori et al. 2006). One inducer of parthenogenetic sea star development is 1-methyladenine (1-MA), which is released by sea star ovarian follicle cells in nature to induce the resumption of meiosis and maturation of oocytes, and can be used in vitro to induce ovulation and spawning behavior (Doreé & Guerrier 1975; Picard & Doreé 1983; Aisenshtadt & Vassetzky 1986; Strathmann 1987; Yoshikuni et al. 1988). The earliest reports of sea star parthenogenesis in California populations of Patiria miniata BRANDT 1835, by Loeb (1913) and Newman (1921), predate the discovery of the hormonal basis of sea star oocyte maturation. Newman (1921) observed parthenogenesis in oocytes of P. miniata that were induced to mature by simple mechanical stimulation of ovaries. A small percentage of mature eggs formed vitelline envelopes without further development, and a highly variable (B1–75%) proportion of eggs without envelopes formed cleavage-stage embryos much later than normally fertilized eggs. All of these parthenogens failed to develop normally for longer than B30h (at laboratory temperatures of 161–191C) or beyond the gastrula embryo stage (Newman 1921). In the course of carrying out laboratory fertilization experiments using adults of P. miniata induced to spawn by 1-MA injection (Strathmann 1987), we have also frequently observed spontaneous formation of vitelline envelopes in a variable but sometimes high percentage of unfertilized eggs, and a small percentage of unfertilized eggs that undergo slow but Invertebrate Biology 128(3): 276–282. r 2009, The Authors Journal compilation r 2009, The American Microscopical Society, Inc. DOI: 10.1111/j.1744-7410.2008.00165.x Author for correspondence. E-mail: [email protected] normal embryogenesis. Here we extend Newman’s original observations in three new directions: (1) the ontogenetic extent of parthenogenetic development is much greater than observed by Newman (1921) and includes functional feeding larval stages; (2) parthenogens occur among offspring of adults from genetically divergent populations of P. miniata (J. Sunday, unpubl. data), including those at the far northern end of the species geographic range; (3) patterns of allelic inheritance within families of parthenogens of P. miniata are consistent with a specific form of naturally occurring parthenogenesis (automixis), and differ from the ploidy changes observed in chemically induced parthenogens in other experimental studies. We discuss these observations of facultative parthenogenesis in P. miniata relative to the evolution of obligate forms of reproduction without outcrossing in closely related asterinid species.