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Unequal Transmission of Mitochondrial Haplotypes

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vol. 161, no. 1 the american naturalist january 2003Unequal Transmission of Mitochondrial Haplotypes in NaturalPopulations of Field Mice with XY Females (Genus Akodon)Hopi E. Hoekstra*Department of Zoology and Burke Museum, University ofWashington, Seattle, Washington 98195Submitted November 12, 2001; Accepted June 29, 2002;Electronically published December 30, 2002abstract: In species with fertile XY females, such as South Amer-ican field mice (genus Akodon), there are two types of mitochondrialDNA (mtDNA), one passing from XX females and one from XYfemales. The XX mothers pass their mtDNA to their XX daughters.The XY mothers, however, produce both XX and XY daughters.Because of this breeding scheme, the XY mtDNA remains isolatedwhereas the XX lineage is continuously invaded by XY mtDNA hap-lotypes. Using a set of recursion equations, I predicted that XYmtDNA haplotypes should rapidly spread through entire populationscomposed of both XX and XY females. I examined patterns of nu-cleotide polymorphism and divergence from the mtDNA controlregion as well as phylogenetic patterns for evidence of an mtDNAsweep. I compared patterns in two sister species, Akodon boliviensisand Akodon azarae, that are composed of 35% and 10% XY females,respectively. Akodon boliviensis XY females are found in all clades ofa phylogenetic mtDNA tree consistent with the spread of mtDNAhaplotypes. In addition, A. azarae mtDNA haplotypes showed nodeviations from neutrality. These results, in combination with highlevels of mtDNA nucleotide diversity in XY females, suggest an an-cient origin (1104generations) of XY females in both A. boliviensisand A. azarae.Keywords: mitochondrial DNA, natural selection, meiotic drive, XYfemales, sex chromosomes, Akodon.Many recent studies have identified regions of the genomethat are influenced by balancing, purifying, or directionalselection (e.g., Hughes and Nei 1989; Tanaka and Nei 1989;McDonald and Kreitman 1991). Such studies use neutralevolution as a null hypothesis to statistically detect selec-* Present address: Department of Ecology and Evolutionary Biology, Bio-Sciences West Building, University of Arizona, Tucson, Arizona 85721; e-mail:[email protected] Nat. 2003. Vol. 161, pp. 29–39. 䉷 2003 by The University of Chicago.0003-0147/2003/16101-010393$15.00. All rights reserved.tion or the unequal transmission of alleles at the molecularlevel (Kimura 1968, 1983). Mitochondrial DNA (mtDNA)in particular has been the focus of many studies of non-neutral evolution (e.g., Nachman et al. 1996). In manycases deviations from neutrality have been detected in themtDNA of a variety of organisms (Nachman 1998; Randand Kann 1998). However, in general the cause andstrength of selection or unequal transmission is obscureand the effects of genotypic differences on individual fit-ness are often unknown. Generally such explanations ofselection are ad hoc. Ideally, one would predict a priorithat patterns at the level of the organism should result inunequal transmission of alleles at a particular locus andthen test that prediction using empirical data. Here I ex-amined a system in which such predictions are possibleas well as quantifiable, and deviations from neutral evo-lution are expected because of the unique breeding systemsof XX and XY females. Ultimately, these theoretical ex-pectations can be used to estimate the age of XY females.In several species of South American field mice (genusAkodon), fertile XY females exist along with wild-type XXfemales in natural populations. In mammals, the male sexis determined by the presence of a functional Y chro-mosome whereas the default phenotype is female. In thiscase, XY females result from a mutation to the Y chro-mosome, which in females is referred to as Y∗to indicateits inability to function properly in male sex determination(Lizarralde et al. 1982; Vitullo et al. 1986; Bianchi et al.1993; Espinosa and Vitullo 1996). XY∗females haveevolved independently in each of six species known tocontain XY∗females and occur at varying frequenciesalong with normal XX females (Hoekstra and Edwards2000). These two genotypic races of females produce twotypes of mtDNA haplotypes: haplotypes derived from XXancestors and those derived from the XY∗ancestor. XXmothers pass their mtDNA haplotypes to their XX daugh-ters, but XY∗mothers pass their mtDNA to both genotypesbecause they produce both XY∗and XX daughters (fig. 1).While litter size is the same for both XX and XY∗females,XY∗females produce female-biased litters because of theloss of YY∗zygotes (Lizarralde et al. 1982; Espinosa 1991;30 The American NaturalistFigure 1: Diagram of breeding scheme and frequencies of females and mtDNA haplotypes. Open circles represent XX mtDNA haplotype; filledcircles represent XY∗mtDNA haplotype. Numbers represent relative frequency of females. The table on the right shows the change in frequency ofmtDNA haplotypes each generation given the frequencies of the XX and XY∗females and equal starting frequencies.Espinosa and Vitullo 1996; Hoekstra and Hoekstra 2001);this provides a transmission advantage to mtDNA hap-lotypes because XY∗mothers produce relatively moredaughters (fig. 1). Finally, XY∗females have a higher re-productive output relative to their XX counterparts (Es-pinosa and Vitullo 1996; Hoekstra and Hoekstra 2001).Because of this breeding scheme, the XX lineage is con-tinuously invaded by mtDNA haplotypes originating fromXY∗females.In this study I examined two sister species, Akodon bo-liviensis and Akodon azarae, in which XY∗females occurat 35% and 10%, respectively (Hoekstra and Edwards2000). On the basis of the transmission dynamics of twocompeting types of mtDNA, I used a recursion model topredict the dynamics of mtDNA evolution in the XX andXY∗mtDNA lineages. I then tested these predictions withempirical data from natural populations to determine howbreeding dynamics translate to variation at the molecularlevel. Specifically, I examined sequences of the mtDNAcontrol region and used both patterns of nucleotide poly-morphism and phylogenetic analysis to detect deviationsfrom neutral expectations. These molecular patterns mayultimately be used to estimate the age of XY∗females ineach species.Model PredictionsI explored the change in frequencies of XX and XY∗mtDNA haplotypes following the origin of the Y∗chro-mosome using a set of recursion equations. It is importantto note that this model considers both


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