Unequal Transmission of Mitochondrial Haplotypes in Natural Populations of Field Mice with XY Females (Genus Akodon)

vol. 161, no. 1 the american naturalist january 2003 Unequal Transmission of Mitochondrial Haplotypes in Natural Populations of Field Mice with XY Females (Genus Akodon) Hopi E. Hoekstra* Department of Zoology and Burke Museum, University of tion or the unequal transmission of alleles at the molecular Washington, Seattle, Washington 98195 level (Kimura 1968, 1983). Mitochondrial DNA (mtDNA) in particular has been the focus of many studies of non- Submitted November 12, 2001; Accepted June 29, 2002; Electronically published December 30, 2002 neutral evolution (e.g., Nachman et al. 1996). In many cases deviations from neutrality have been detected in the mtDNA of a variety of organisms (Nachman 1998; Rand and Kann 1998). However, in general the cause and strength of selection or unequal transmission is obscure abstract: In species with fertile XY females, such as South Amer- and the effects of genotypic differences on individual fit- ican field mice (genus Akodon), there are two types of mitochondrial DNA (mtDNA), one passing from XX females and one from XY ness are often unknown. Generally such explanations of females. The XX mothers pass their mtDNA to their XX daughters. selection are ad hoc. Ideally, one would predict a priori The XY mothers, however, produce both XX and XY daughters. that patterns at the level of the organism should result in Because of this breeding scheme, the XY mtDNA remains isolated unequal transmission of alleles at a particular locus and whereas the XX lineage is continuously invaded by XY mtDNA hap- then test that prediction using empirical data. Here I ex- lotypes. Using a set of recursion equations, I predicted that XY amined a system in which such predictions are possible mtDNA haplotypes should rapidly spread through entire populations as well as quantifiable, and deviations from neutral evo- composed of both XX and XY females. I examined patterns of nucleotide polymorphism and divergence from the mtDNA control lution are expected because of the unique breeding systems region as well as phylogenetic patterns for evidence of an mtDNA of XX and XY females. Ultimately, these theoretical ex- sweep. I compared patterns in two sister species, Akodon boliviensis pectations can be used to estimate the age of XY females. and Akodon azarae, that are composed of 35% and 10% XY females, In several species of South American field mice (genus respectively. Akodon boliviensis XY females are found in all clades of Akodon), fertile XY females exist along with wild-type XX a phylogenetic mtDNA tree consistent with the spread of mtDNA females in natural populations. In mammals, the male sex haplotypes. In addition, A. azarae mtDNA haplotypes showed no deviations from neutrality. These results, in combination with high is determined by the presence of a functional Y chro- levels of mtDNA nucleotide diversity in XY females, suggest an an- mosome whereas the default phenotype is female. In this cient origin (1104 generations) of XY females in both A. boliviensis case, XY females result from a mutation to the Y chro- and A. azarae. mosome, which in females is referred to as Y∗ to indicate its inability to function properly in male sex determination Keywords: mitochondrial DNA, natural selection, meiotic drive, XY (Lizarralde et al. 1982; Vitullo et al. 1986; Bianchi et al. females, sex chromosomes, Akodon. 1993; Espinosa and Vitullo 1996). XY∗ females have evolved independently in each of six species known to contain XY∗ females and occur at varying frequencies Many recent studies have identified regions of the genome along with normal XX females (Hoekstra and Edwards that are influenced by balancing, purifying, or directional 2000). These two genotypic races of females produce two selection (e.g., Hughes and Nei 1989; Tanaka and Nei 1989; types of mtDNA haplotypes: haplotypes derived from XX McDonald and Kreitman 1991). Such studies use neutral ancestors and those derived from the XY∗ ancestor. XX evolution as a null hypothesis to statistically detect selec- mothers pass their mtDNA haplotypes to their XX daughters, but XY∗ mothers pass their mtDNA to both genotypes * Present address: Department of Ecology and Evolutionary Biology, Bio- ∗ Sciences West Building, University of Arizona, Tucson, Arizona 85721; e-mail: because they produce both XY and XX daughters (fig. 1). ∗ [email protected]. While litter size is the same for both XX and XY females, ∗ Am. Nat. 2003. Vol. 161, pp. 29–39. ᭧ 2003 by The University of Chicago. XY females produce female-biased litters because of the ∗ 0003-0147/2003/16101-010393$15.00. All rights reserved. loss of YY zygotes (Lizarralde et al. 1982; Espinosa 1991; 30 The American Naturalist Figure 1: Diagram of breeding scheme and frequencies of females and mtDNA haplotypes. Open circles represent XX mtDNA haplotype; filled circles represent XY∗ mtDNA haplotype. Numbers represent relative frequency of females. The table on the right shows the change in frequency of mtDNA haplotypes each generation given the frequencies of the XX and XY∗ females and equal starting frequencies. Espinosa and Vitullo 1996; Hoekstra and Hoekstra 2001); pinosa and Vitullo 1996). As a consequence, XY∗ mothers this provides a transmission advantage to mtDNA hap- produce on average four-thirds times as many daughters lotypes because XY∗ mothers produce relatively more as an XX mother. When we consider maternally inherited daughters (fig. 1). Finally, XY∗ females have a higher re- mtDNA haplotypes, males represent an evolutionary “dead productive output relative to their XX counterparts (Es- end” and are therefore not considered here. Importantly, pinosa and Vitullo 1996; Hoekstra and Hoekstra 2001). XX daughters produced by an XY∗ mother will produce Because of this breeding scheme, the XX lineage is con- half daughters and half sons (just as an XX daughter de- tinuously invaded by mtDNA haplotypes originating from rived from an XX mother), so the XY∗ haplotype will not XY∗ females. be passed down multiplicatively in this lineage (fig. 1). In this study I examined two sister species, Akodon bo- Because XY∗ mothers produce more daughters than XX liviensis and Akodon azarae, in which XY∗ females occur females, the XY∗ mtDNA haplotype has a transmission at 35% and 10%, respectively (Hoekstra and Edwards advantage. In addition to producing proportionately more 2000). On the basis of the transmission dynamics of two daughters because of compensation, XY∗ mothers have an competing types of mtDNA, I used a recursion model to added reproductive advantage: XY∗ mothers have a longer predict the dynamics of mtDNA evolution in the XX and reproductive life and the interval between litters is reduced XY∗ mtDNA lineages. I then tested these predictions with (Espinosa 1991; Espinosa and Vitullo 1996). empirical data from natural populations to determine how Previous work suggests that meiotic drive may also be breeding dynamics translate to variation at the molecular operating in this system (Hoekstra and Hoekstra 2001). level. Specifically, I examined sequences of the mtDNA Transmission bias favoring the Y∗ chromosome over the control region and used both patterns of nucleotide poly- X results in unequal transmission of the XY∗ mtDNA in morphism and phylogenetic analysis to detect deviations XY∗ litters because those loci are jointly inherited. A value from neutral expectations. These molecular patterns may of meiotic drive found in XY∗ females favoring the Y∗ ∗ ultimately be used to estimate the age of XY females in chromosome over the X (d p 0.264 ; i.e., the Y∗ chro- each species. mosome is transmitted 76.4% of the time and the X chromosome 23.7% of the time) and a value for male meiotic drive favoring the Y chromosome over the X (g p 0.1 ; Model Predictions i.e., the Y chromosome is transmitted 60% of the time I explored the change in frequencies of XX and XY∗ and the X chromosome 40% of the time), which equalizes mtDNA haplotypes following the origin of the Y∗ chro- the sex ratio, are incorporated into the model. Similarly, mosome using a set of recursion equations. It is important a relative reproductive fitness estimate (q p 1.15 ) favoring to note that this model considers both compensation for XY∗ females was used. Similar values were estimated using loss of YY∗ zygotes and the relative reproductive fitness reproductive data from a laboratory colony of A. azarae difference between XX and XY∗ females as observed in and are reported in Hoekstra and Hoekstra (2001). It is Akodon azarae.XY∗ females “compensate” for YY∗ zygotes important to note that the prediction of the XY∗ mtDNA that are inviable by producing more ovules than implant, spread holds regardless of the exact parameter values; equalizing litter sizes between XX and XY∗ mothers (Es- rather, the parameters influence the rate of the sweep. Unequal Transmission of mtDNA Haplotypes 31 to XX females),d p meiotic drive in XY∗ females favoring the Y∗ chromosome (transmission frequency 1 0.5), and g p meiotic drive in XY males favoring the Y chromosome (transmission frequency 1 0.5). 1 N (t ϩ 1) p ()1 Ϫ g R # N (t), (1) XX2 XX XX ()1 Ϫ d Ϫ g ϩ dg N ∗(t ϩ 1) p R # N (t), (2) XX()3 Ϫ d Ϫ g Ϫ dg XY XX ()1 ϩ d Ϫ g Ϫ dg N ∗∗(t ϩ 1) p R # N (t). (3) XY()3 Ϫ d Ϫ g Ϫ dg XY XY These numbers (eqq. [1]–[3]) can then be normalized by dividing by the number of all females to obtain relative frequencies of the three genotypes. (1 Ϫ d ϩ g Ϫ dg)1 N (t ϩ 1) p R ϩ (1 ϩ g)R # N (t) XY(3 Ϫ d Ϫ g Ϫ dg)2 XY XX XY (4) By dividing the number of males (eq.

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