Copyright zyxwvutsrqpo 0 I996 by the Genetics Society of zyxwvutsrq America zyxwvutsrqpon Microsatellite and Chromosome Evolution of Parthenogenetic Sitobion Aphids zyxw in Australia Paul Sunnucks, Phillip R. England, Andrea C. Taylor and Dinah F. Hales School of Biologzcal Sciences, Macquarie University, Sydney, New South Wales zyxwv 2109, Australia Manuscript received March 19, 1996 Accepted for publication July zyxwvu 5, 1996 ABSTRACT Single-locus microsatellite variation correlated perfectly with chromosome number in Sitobion miscanthi aphids. The microsatellites were highly heterozygous, with up to 10 alleles per locus in this species. Despite this considerable allelic variation, only seven different S. miscanthi genotypes were discovered in 555 individuals collected from a wide range of locations, hosts and sampling periods. Relatedness between genotypes suggests only two successful colonizations of Australia. There was no evidence for genetic recombination in 555 S. miscanthi so the occurrence of recent sexual reproduction must be near zero. Thus diversification is by mutation and chromosomal rearrangement alone. Since the aphids showed no sexual recombination, microsatellites can mutate without meiosis. Five of seven microsatellite differences were a single repeat unit, and onelarger jump is likely. The minimum numbers of changes between karyotypes corresponded roughly one-to-one with microsatellite allele changes, which suggests very rapid chromosomal evolution. A chromosomal fission occurred in a cultured line, and a previously unknown chromosomal race was detected. All 121 diverse S. nearfragariaewere heterozygous but revealed only one genotype. This species too must have a low rate of sexual reproduction and few colonizations of Australia. I NVESTIGATIONS of parthenogenetic organisms are a powerful approach to understand many funda- mental aspects of genetics, including the generation and maintenance of genetic variation, mechanisms of mutation and chromosomal change, and roles of ge- netic linkage in shaping phenotypes (HUGHES 1989). Taxa in which different modes of reproduction occur may be particularly enlightening, where it is possible to separate factors that are confounded in other organ- isms. Relatively few groups of organisms exhibit a range of modes of reproduction and also fulfillpractical con- siderations allowing hypothesis testing. Cladocerans are one such group; their genetics have been well-studied, with important advances in the understanding of ge- netic structure and function (e.g., HEBERT et al. 1989; VAN RAAY and CREASE 1995).Aphids are equally promis- ing, because of the large number of species and varia- tion in life histories. Aphid reproduction encompasses obligate and facultative apomictic parthenogenesis and holocycly (a sexual phase once a year, with many in- tervening parthenogenetic generations), and some- times this range can occur within species (HALES et al. 1996). The maturation of an egg under apomictic partheno- genesis is ameiotic, with the chromosomes undergoing essentially a mitotic division, producing true clones (re- viewed by BIACKMAN 1987). All offspring are genetically Corre$mnding author: Paul Sunnucks, School of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia. E-mail: psunnuck@rna.hio.mq.edu.au Genetics 144: 747-756 (October-, 1996) identical except for mutations, chromosomal rear- rangements, and perhaps rare mitotic recombination events. There are many important genetic conse- quences of these facts (review in HUGHES 1989; HALES et al. 1996). First, apomictic lineages inherit their genetic information as one linkage group. Thus apomixis should promote adaptive gene complexes, but it may also allow accumulation of deleterious mutations. Sec- ond, genetic variation arises by mutation and chromo- somal rearrangement alone, rather than by genetic re- combination. This will affect the type, pattern and rate of production of genetic variation. In particular, chro- mosomal rearrangements are relatively common in aphids, probably because hemipteran chromosomes have no localized centromere, and in parthenogenetic lineages there is no evolutionary constraint on chromo- somal rearrangement associated with meiosis. Several aphid chromosomal rearrangements are associated with radical new genotypes including insecticide resis- tance and host specificity (BLACKMAN et al. 1978, 1995; BROWN and BLACKMAN 1988; DEVONSHIRE 1989). Because ofthe range of important genetic and evolu- tionary questions that can be approached in aphids, we are investigating the populationgenetics, chromosomal evolution, and ecological adaptation of aphid model species in the genus Sitobion. We have developed sin- gle-locus microsatellites for use in this research pro- gram. Microsatellites in insects and other organisms show a wide range of gene diversity, are codominant, and are relatively free of natural selection (BRUFORD and WAYNE 1993; HUGHES and QUELLER 1993; ESTOUP Downloaded from https://academic.oup.com/genetics/article/144/2/747/6016948 by guest on 03 September 2021