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Triploid Gynogenetic Fish Clones ( Poeciliopsis : Poeciliidae )
| Content Provider | Semantic Scholar |
|---|---|
| Author | Joseph Quattro Robert Vrijenhoek |
| Copyright Year | 2002 |
| Abstract | Most tributaries of the Rio Fuerte in northwestern Mexico contain one or more clones of allotriploid fish of the genus Poeciliopsis. We used multilocus allozyme genotypes and mitochondrial DNA (mtDNA) haplotypes to examine several potential modes of origin of these gynogenetic all-female fish. The allozyme studies corroborated earlier morphological work revealing the hybrid constitution of two triploid biotypes, Poeciliopsis 2 monacha-lucida and Poeciliopsis monacha-2 lucida. Each biotype carries one or two whole genomes from the each of the sexual species P. monacha and P. lucida. Restriction site analysis of mtDNA revealed that P. monacha was the maternal ancestor of five electrophoretically distinguishable triploid clones. Four f five clones were marked by closely related, composite, allozymefmtDNA genotypes, suggesting they had common origins from an allodiploid clone of the P. monacha-lucida biotype. Genotypic analysis revealed that all five clones arose via the “genome addition” pathway. Fertilization of unreduced ova in P. monacha-lucida females by sperm from P. monacha and P. lucida males, respectively, gave rise to both biotypes. A PPROXIMATELY 70 clonally reproducing, vertebrate biotypes have been identified. Essentially all are hybrids between two or more biparentally reproducing sexual species, and the majority (64%) are polyploid (VRIJENHOEK et a l . 1989). Based on studies with unisexual fishes of the genus Poeciliopsis SCHULTZ (1969) first postulated that a relationship exists between hybridization, unisexuality, and polyploidy in vertebrates. He suggested that normal meiotic processes often are disrupted in interspecific hybrids. Occasionally, these hybrids produce unreduced ova (AB) that, upon backcrossing with one of the sexual ancestors (species A or B), lead to new polyploid (allotriploid) biotypes (AAB and ABB). We refer to this pathway for the origin of allotriploid biotypes from allodiploid ancestors as the “genome addition” hypothesis. Based on cytogenetic studies of meiosis in unisexual Poeciliopsis, CIMINO (1972a) considered a variety of pathways for the origin of allopolyploid vertebrates. For example, under what we will refer to as the “genome duplication” hypothesis, suppression of an equational division in an AB hybrid could produce unreduced AA or BB ova which, if fertilized by species A or B, would produce AAB or ABB offspring. Autopolyploid, AAA and BBB, progeny also would result from this process, but self-sustaining populations of autopolyploid unisexual vertebrates have not been found. ' Present address: Hopkins Marine Station, Stanford University, Pacific Grove, California 93950. Genetics 130: 621-628 (March, 1992) Both the “genome addition” and “genome duplication” hypotheses assume that allotriploids arise from preexisting allodiploid ancestors. The existence of allodiploid relatives to many triploid biotypes lends credence to this assumption. For some triploids, however, self-sustaining allodiploid relatives have not been identified, for example: carp (genus Carassius), salamanders (Ambystoma), gekkonid lizards (Hemidactylus and Heteronotia), agamid lizards (Leiolepis), and some teiid lizards (Cnemidophorus); see VRIJENHOEK et al. (1989). Either the allodiploid ancestors were unstable and could not persist longer than one or a few generations, or perhaps they never existed. CUELLAR (1974, 1977) advanced a third, nonhybrid, pathway, referred to as the “spontaneous origin” hypothesis. He suggested that occasional parthenogenetic reproduction is an inherent property of the sexual progenitors. Thus, species A would be capable of producing unreduced ova (AA) that develop spontaneously. To explain the hybrid genotypes of many parthenogenetic lizards, CUELLAR argued that hybridization might be involved as a secondary process. Occasional fertilization of unreduced AA ova by species B would produce an allotriploid AAB. He criticized the hybrid origin pathways advanced by SCHULTZ and CIMINO, because the putative allodiploid ancestors of triploid Poeciliopsis exhibited an oogenetic process (hybridogenesis, involving premeiotic exclusion of the paternal genome, see below) that bore no cytological resemblance to that of the triploids (gynogenesis, characterized by premeiotic doubling, 622 J. M. Quattro, J. C . Avise and R. C. Vrijenhoek see below), thereby providing no mechanistic link between them. Modern genetic techniques offer an opportunity to discriminate among these hypothetical pathways. Comprehensive allozyme surveys of unisexual populations and their closest sexual relatives have corroborated that essentially all unisexual vertebrates are interspecific hybrids (DAWLEY 1989). Furthermore, studies of maternally inherited mitochondrial DNA (mtDNA) reveal that hybrid origins typically are asymmetrical, occurring in one direction only (e .g . , AP X Bb males us. Bo X Ab) (BROWN and WRIGHT 1979; AVISE and VRIJENHOEK 1987; MORITZ et al. 1989). mtDNA analysis has been used to refute the “spontaneous-origins” hypothesis for several parthenogenetic lizards (DENSMORE et al. 1989; MORITZ, WRIGHT and BROWN 1989). If parthenogenetic lizards arose spontaneously from sexual ancestors and hybridization was secondarily involved (CUELLAR'S “spontaneous origins” hypothesis), the paired-homospecific genomes should derive from the maternal parent, and thus should be coupled with mtDNA from the same species (i.e., AA genomes of AAB should be coupled with mtDNA type-A, and vice versa for ABB). Eight of 10 parthenogenetic Cnemidophorus species did not reveal the predicted coupling. Conversely, hybrid origins followed by genome addition or duplication could give rise to either ABB-mtDNAA or ABB-mtDNAB, depending on which genome was duplicated or added. Assuming hybrid origins, genome addition can be discriminated from genome duplication by the presence or absence of heterozygosity in the homospecific pair of genomes (VRIJENHOEK 1990). For example, genome duplication would result in triploids that are homozygous for all genes carried by the homospecific pair of genomes (A'A'B). Alternatively, genome addition will result in heterozygosity for many loci carried by the homospecific pair of genomes (A'A2B). Postformational mutations will also contribute to homospecific heterozygosity, so the analysis must be restricted to alleles that are polymorphic in the sexual ancestors. Unequivocal evidence for evolution by genome addition exists in trihybrid unisexuals (ABC) that comprise the genomes of three species, such as Poeciliopsis monacha-lucida-viriosa (SCHULTZ 1977) and Cnemidophorus exsanguis (GOOD and WRIGHT 1984). The present study used allozyme and mtDNA analysis to discriminate among possible modes of origin of triploid forms of Poeciliopsis inhabiting the Rio Fuerte drainage of northwestern Mexico. Each triploid is a hybrid, containing genomes from two sexually reproducing species, P. monacha and P. lucida. One triploid biotype, P. 2 monacha-lucida (to which we refer as MML), has two monacha genomes and one from lucida; and the other, P. monacha-2 lucida (MLL), has two lucida genomes and one from monacha (SCHULTZ 1969). Both biotypes reproduce by gynogenesis, a clonal mechanism that faithfully replicates the entire triploid genome across generations (SCHULTZ 1967). CIMINO (1972b) showed that the entire triploid genome is replicated during an endomitotic event prior to meiosis. Pairing of replicated chromosomes followed by normal reductional and equational divisions results in production of nonrecombinant triploid ova. Sperm from a coexisting host species (P. monacha for MML and P. lucida for MLL) is required to activate embryogenesis of triploid eggs, but paternal genes make no contribution to the allfemale offspring. SCHULTZ (1969) proposed that both triploid biotypes arose via genome addition from the hybridogenetic biotype P. monacha-lucida (ML). Hybridogenesis is a hemiclonal form of reproduction; only the haploid M genome is transmitted to developing ova. Apparently, M chromosomes selectively attach to a unipolar spindle during a premeiotic cell division, and L chromosomes are discarded prior to the opportunity for synapsis or recombination (CIMINO 1972a). Normal meiosis ensues with a single equational division producing haploid M ova. Fertilization of these ova by L sperm from P. lucida males restores diploidy and the ML genotype. Both maternal and paternal traits are expressed in the allodiploid progeny. Because of the cytological differences between hybridogenesis and gynogenesis, it might be unwarranted to assume that all triploid forms of Poeciliopsis arose from allodiploid unisexuals (CUELLAR 1977). An additional complication exists because both the MML and MLL biotypes comprise several clones that are distinguishable on the basis of allozyme genotypes, histocompatibility differences, and ecological characteristics (MOORE 1977; VRIJENHOEK 1978; SCHULTZ 1982; SCHENCK and VRIJENHOEK 1989). Different clones of a particular biotype (e.g., MML/I us. MML/ XI, Roman numerals designate distinguishable electromorph or “E-type” clones) might have had independent origins by entirely different pathways. The present results clearly refute both the “spontaneous origins” and “genome duplication” hypotheses for the evolution of these two biotypes. Only SCHULTZ'S (1 969) “genome addition” hypothesis is consistent with the combined allozyme and mtDNA data for all five clonal strains examined in this study. MATERIALS AND METHODS Comprehensive allozyme surveys have not been reported for allotriploid Poeciliopsis. Allozyme surveys have been in progress for the past 18 years, and include genotypes for several thousand sexual and unisexual Poeciliopsis from the Rio Fuerte, and adjacent rivers to the north (Rio Mayo) and south (Rios Sinaloa and Mocorito). Unfortunately, these individuals were preserved in a manner making them unEvolution of Triploid Poeciliopsis 623 |
| File Format | PDF HTM / HTML |
| Alternate Webpage(s) | https://escholarship.org/content/qt6vx7t427/qt6vx7t427.pdf?t=q1zojo |
| Language | English |
| Access Restriction | Open |
| Content Type | Text |
| Resource Type | Article |
