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Is the Female Biased Sex Ratio in Wood Lemming Myopus Schisticolor Maintained by Cyclic Inbreeding?

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Is the Female Biased Sex Ratio in Wood Lemming Myopus Schisticolor Maintained by Cyclic Inbreeding? OIKOS 30: 89-89. Copenhagen 1978 Is the female biased sex ratio in wood lemming Myopus schisticolor maintained by cyclic inbreeding? Nils Chr. Stenseth Zoological Institute, University of Oslo Stenseth, N. C. 1978. Is the female biased sex ratio in wood lemming Myopus schisticolor maintained by cyclic inbreeding?- Oikos 30: 83-89. The hypothesis is developed where the female biased sex ratio in wood lemming Myopus schisticolor (Lillj.), a cyclic microtine, is maintained through evolutionary time by recurrent inbreeding. If the effects, with respect to sex ratio, of inbreeding are stronger than the effects of outbreeding, then the optimal strategy (being favour­ ed by individual selection) would be to produce as many females as possible; the condition is that a sufficient number of males are present to ensure fertilization of all (or most) daughters. This is ensured by producing enough sons and/or by fathers mating with daughters. Some evidence supporting the occurrence of cyclic inbreeding (both sister-brother and daughter-father matings) during large fractions of microtine cycles in general, is outlined. Female biased sex ratio is predicted to be more common among exaggerated cyclic microtines than appreciated at present. One known case that seems to be similar to the situation in the wood lemming is briefly discussed: The arctic lemming Dicrostonyx torquatus (Pall.) in arctic USS R and North America. Studies aimed at producing data for testing the hypothesized occurrence of in­ breeding are sorely needed: Microtines should be studied with respect to breeding structure during low and early increase phases. In addition, breeding experiments for analysing the genetic mechanism are needed. N. C. Stenseth, Zoological Institute, P. 0. Box 1050, Blindern, Oslo 3, Norway. 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TeH,D,eHIJ.I1H K npeo6JlaJ1aHI1''l CaMOK B nOny.rnruHI1 KCI)KeTC5I 5o­ nee oe't>Jt.HoA cpemr Ml1KPJTHH c UHKJlHtJ:eCJ<HM pa3BI1TI!eM '!eM C'IHTaeTCH. KpaT­ KO OnHCaH O,D,HH 113BeCT� CJlYt{aH no-B� CXO� C CWI'YaJ.le� Y neM­ MHHrGB I<O�Horo JleMMHHra Diar>ostonyx tor>quatus (Pall . ) a apKTHtJ:eCKHX pal1oHax CCCP H Cea • M£pHKH. Heooxo,I:�,HM: Hccne.n.oBaHHH c UeJlb"' npo,I: .D.aH� )l1 onpe,neneHI15I rHOOTeTHt.IeCJ<oro Ha.J1!1tlH 11H6p�Hra: MHKPJTI!Hbl ,D,OJlJKHbl 6brh HCCJle,D,OBaHbl C yqeTa-1 CTpYKTYP:>J pa3MHO)KeHI1H B TetieHHe ¢a3 HH3I<OA qHcneHHOCTH H ee noBblHHH. KpcMe Toro 1 Heo6XO.D.l'!M rrae.r:r.eHHe o�oa no pa3MHO>KeHH!'l ,D,rni aHaJl13a reHeTHtieCJ<oro MexaHI13!vla. Accepted 23 August 1977 © OIKOS OIKOS 30:1 (1978) 83 6• 1976), the observations of Wachtel and his co-workers 1. Introduction indicate that the Y-gene(s) either is (are) absent, or not The wood lemming Myopus schisticolor (Lilljeborg), a operating in XY females. cyclic microtine (cf. Krebs and Myers 1974), has been Fredga and his co-workers hypothesized that (1) reported to have a female biased sex ratio (20 to 30% there is an X-linked factor (or gene, called X* whene ver males) under both laboratory and field conditions (Ka­ necessary in the following) which represses the male lela and Oksala 1966, Frank 1966, Fredga et al. 1976, determining effect of the Y -chromosome; (2) this 1977). Breeding experiments in the laboratory show X-linked factor is transferred by the XY -females to all that a significant proportion of the females produce only of their eggs, presumably by the operation of a meiotic daughters. There is some indication that this sex ratio drive (Sandler and Novitski 1957) causing mainly distortion may be ancient (cf. Fredga et al. 1976) and X-carrying eggs to be produced. Thus mainly (or only, if consequently evolutionarily stable. However, from Fis­ the meiotic drive is 100% effective) female offspring her (1930) an approximately 1:1 sex ratio is, under result. Clearly, a population where X* has gone to fixa. most circumstances, expected to be the only evolution­ tion is dead; there will be no male in such a population. arily stable ratio. I contend that the Fisherian argument Thus, a polymorphism is expected. does not apply to the wood lemming. It should be pointed out that Fredga and his co-work. Specifically, the purpose of this paper is to present, in ers do not show any evidence, other than circumstantial, qualitative terms, an evolutionary mechanism for the for the existence of a mutant X gene. Thus, the mutant maintenance of this female biased sex ratio (Sect. 3). gene suppressing the male determining genes on they Only circumstantial evidence for the validity of the hy­ chromosome might equally well be on an autosomal pothesis is presented. (Sect. 4). However, based on the chromosome. However, Bengtsson (1977) gives strong analysis of Maynard Smith and Stenseth (1978) I con­ reasons to believe that the mutant gene is unlikely to be sider the hypothesis a plausible one for the wood lem­ an autosomal one. Thus, Bengtsson (1977: 339) de­ ming. monstrates that an autosomal sex reversal gene, A* will Secondly, I present a general hypothesis stating that always be selected against and will disappear from the cyclic microtines may be expected to have female biased population under the condition that the sex reversed sex ratios at birth. However, I do not maintain that the animals have lower fertility than other animals. What specific genetic mechanism seen in wood lemmings will happen if such a reduced fertility is not connected (Sect. 2; leading to extreme sex ratio distortions) is a with sex reversal remains to be analyzed. The general general one. hypothesis presented below, for the evolutionary Thirdly, I point out some important, but poorly un­ maintenance of the female biased sex ratios applies derstood aspects of micro tine population biology. As whether the sex reversing gene is autosomal or not. done by Krebs and Myers (1974), the following discus­ In a population with X*, X, and Y, three types of sion points to the importance of studying cyclic microti­ matings are possible: nes also when they are rare. XX S?x XY d giving 1 S? : 1 cJ X*X S?x XY d giving 3 S?S?: 1cJ' 2. Genetic mechanism X*Y S?x XY d giving only � � Fredga et al. (1976, 1977) have recently reported that some females, producing mainly female offspring, had Bengtsson (1977) has shown that in a random mating an XY chromosome constitution. Otherwise both XX population the frequencies of the four different geno· and XY females seem to be phenotypically indistin­ types X*X, XX, X*Y, and XY all are expected to be guishable. No difference in litter size was found. Kalela close to 0.25. Thus, there will be approximately 25% and Oksala (1966) report observations from laboratory males in the population. Simulations indicate that this experiments that can be interpreted as XY females result does not depend on whether or not inbreeding · having a mean litter size equal to 3.94 ± 0.18 (based on occurs (Maynard Smith and Stenseth 1978); the only 89 litters from 18 different females) whereas the other condition is that all females are potentially mated. This · females (i.e.XX which actually may be of two genetic­ latter condition is likely to be valid, an inference ba sed ally different types, see below) had a mean litter size on the observed greater home range of males compa red 1 equal to 4.00 ± 0.16 (based on 111 litters from 26 with females in many microtine species (e.g. Myllymiiki different females). 1975). Furthermore, Skaren (1964) observed 100% • Furthermore, Wachtel et al. (1976) have demon­ pregnancy among wild caught wood lemmings. Thus, strated that XY females are H-Y antigen negative while Fredga and his co-workers' hypothesis may be conclud· · XY males are H-Y antigen positive ( cf. Silvers and ed to result in an ecologically stable system in a global Wachtel 1977). Presuming that the H-Y antigen is the sense. This is an important property of a genetic system gene product of the Y chromosome, responsible for ini­ to operate in cyclic fluctuating species like the wood · tiating testicular differentiation and male development lemming: The frequencies of the different genotypes Ii: (cf. Bmgger and Aagenres 1964, Crew 1965, Ohno a population may be radically changed due to migratien 84 OIKOS 30:1 (19.1$) (the tendency to disperse seems to be unevenly distri­ and genes determining the sex of the individual, will buted over different genotypes (cf. Krebs et al. 1973)), tend to produce a 1:1 sex ratio at birth. The only genes or due to drift and founder effects (which might be of distorting sex ratio, which would at first be selected, are great importance just after the crash).
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