Neo-Y Chromosome of Drosophila americana amemkana

The extent of genetic degeneration of the nec-Y chromosome of Drosophila americana ama'cana has been investigated. Three loci, coding for the enzymes enolase, phosphoglycerate kinase and alcohol dehydrogenase, have been localized to chromosome 4 of D. a. americunu, which forms the neo-Y and neo-X chromosomes. Crosses between D. a. americana, and D. virilis or D. montana showed that the loci coding for these enzymes carry active alleles on the neo-Y chromosome in all wild-derived strains of ama'cana that were tested. Intercrosses between a genetically marked stock of virilis and strains of americana were carried out, creating F3 males that were homozygous for sections of the neo-Y chromosome. The sex ratios in the F3 generation of the intercrosses showed that no lethal alleles have accumulated on any of the neo-Ychromosomes tested. There was evidence for more minor reductions in fitness, but this seems to be mainly caused by deleterious alleles that are specific to each strain. A similar picture was provided by examination of the segregation ratios of two marker genes among the Fs progeny. Overall, the data suggest that the neo-Y chromosome has undergone very little degeneration, certainly not to the extent of having lost the functions of vital genes. This is consistent with the recent origin of the neo-Y and neo-X chromosomes, and the slow rates at which the forces that cause Y chromosome degeneration are likely to work. T HE Ychromosomes of many animal and some plant species are genetically degenerate, with few active genes other than those required for functions specific to the heterogametic sex (MULLER 1918; WESTERGAARD 1958; WHITE 1973; BULL 1983; GRAVES 1995). In several groups, it is known that the loss of genetic activity on the Ychromosome has been accompanied by the evolution of dosage compensation, so that equal amounts of X chromosomal gene products are produced in males and females, despite the difference in ploidy level (MULLER 1932; LYON 1961; LUCCHESI 1993). It is clear from comparative evidence that Y chromosome degeneration has evolved independently in several different lineages (BULL 1983), suggesting that relatively simple evolutionary forces are involved. The nature of these forces has been debated for many years. It is generally accepted that Ychromosomes were originally homologous to X chromosomes, and that they have lost genetic activity through the accumulation of deleterious mutations, whose spread at X-linked loci is prevented by selection. The absence of recombination between all or part of the X and Y chromosomes almost certainly plays a major role in promoting the accumulation of deleterious mutations and repetitive DNA sequences on the Y chromosome (MULLER 1918; FISHER 1935; NEI 1970; CHARLESWORTH 1978, 1991, Corresponding author: Brian Charlesworth, Department of Ecology and Evolution, University of Chicago, 1101 E. 57th St., Chicago, IL 60637-1573. E-mail: [email protected] Genetics 145 989-1002 (April, 1997) 1996; LUCCHESI 1978; RICE 1987, 1994; JABLONKA and LAMB 1990). There is currently no agreement on the details of the mechanisms of such accumulation, and no tests of the various hypotheses with data from natural populations have been carried out. As pointed out by LUCCHESI (1978), the neo-X and neo-Y chromosomes of certain members of the genus Drosophila, which are formed by centric fusions between an autosome and a basic X or Y chromosome, provide excellent material for studying intermediate stages of Y chromosome degeneration. The absence of crossing over in male Drosophila means that the homologue of an autosomal arm that becomes fused to the Xchromosome cosegregates with the original Y in male meiosis (provided that disjunction is regular), and hence is inherited in exactly the same fashion as a regular Y chromosome, although it is not physically joined to it. An autosome that is fused to the Ychromosome is obviously inherited together with the Y, while its homologue cosegregates with the X chromosome. In both cases, the neo-Y chromosome has exactly the same nonrecombining and permanently heterozygous status as a regular Y chromosome, although it plays no role in sex determination. It is therefore exposed to the same evolutionary forces that are thought to lead to the degeneration of the original Ychromosome. Genetic investigations of species that have acquired their neo-Ychromosomes at widely different times may therefore shed light on these forces. In species with an ancient neo-Y chromosome, such 990 B. Charlesworth et al. as D. pseudoobscura, the neo-Y chromosome appears to have completely degenerated, and the homologous arm of the neo-X chromosome in males is fully dosage compensated (LUCCHESI 1978, 1993). A more recent event generating a neo-Y chromosome has occurred in the close relative of D. pseudoobscura, D. miranda, as a result of a fusion between the Y chromosome and autosomal element Cof the basic Drosophila karyotype (DOBZHANSKY and TAN 1936; MULLER 1940). In this case, only some of the genes on the neo-Y have lost function, and only part of the homologous arm of the neo-X has responded by becoming dosage compensated (MACKNIGHT 1939; STROBEL et al. 1978; DAS et al. 1982; BONE and KURODA 1996; MAR~N et al. 1996; STEINEMANN et al.