Inheritance of Litter Size at Birth in the Brazilian Grass Mouse (Akodon Cursor, Sigmodontinae, Rodentia)

Genet. Res., Camb. (2002), 80, pp. 55–62. With 1 figure. # 2002 Cambridge University Press 55 DOI: 10.1017\S0016672302005724 Printed in the United Kingdom Inheritance of litter size at birth in the Brazilian grass mouse (Akodon cursor, Sigmodontinae, Rodentia) " # $ " % YU. S. AULCHENKO , L. O. ARARIPE , P. S. D’ANDREA , A. A. SHISHKIN , , # " # % " % R. CERQUEIRA , P. M. BORODIN , , T. I. AXENOVICH , * " Institute of Cytology and Genetics, Russian Academy of Science, 630090 Noosibirsk, Russia # Institute of Biology, Federal Uniersity of Rio de Janeiro, Rio de Janeiro, Brazil $ Institute of Tropical Medicine, Oswaldo Cruz Foundation, Rio de Janeiro, Brazil % Department of Cytology and Genetics, Noosibirsk State Uniersity, 630090 Noosibirsk, Russia (Receied 4 December 2001 and in reised form 10 April 2002) Summary By means of complex segregation analysis we studied the inheritance of litter size in two large pedigrees of captive-bred colonies of the Brazilian grass mouse Akodon cursor. Genetic analysis has revealed a highly significant influence of genetic factors on the variation of litter size (heritability, # h , was estimated as 0n44). The inheritance followed the classical polygene model: neither the major-gene model nor the polygene with unequal contribution model described the data significantly better. them in captivity we may estimate the genetic structure 1. Introduction of the traits. Weigensberg & Roff (1996) demonstrated Analysis of genetic and environmental factors controll- that laboratory estimates of heritability provide ing variation of life history traits in natural popula- reasonable estimates of both the magnitude and the tions is essential to understanding their evolution. significance of heritabilities in nature. However, little is known about the quantitative In this study we use this approach to analyse the genetics of natural populations. A study of genetic genetic control of one of the most important life control requires trait measurements on many indivi- history traits – litter size – in a captive-bred colony of duals of known parentage (Falconer & MacKay, the Brazilian grass mouse Akodon cursor, Winge, 1887 1996; Lynch & Walsh, 1997). Natural populations (Sigmodontinae, Rodentia). rarely provide this opportunity. Although several new Inheritance of litter size has been extensively studied methods of parentity testing have recently been in various laboratory and farm animals (Mafizul developed and applied to field studies (Slate et al., Islam & Hill, 1976; Eklund & Bradford, 1977; Land, 1999; Kruuk et al., 2000; Merila & Sheldon, 2000; 1978; Falconer, 1989; Eisen & Johnson, 1981; Kingsolver et al., 2001), the progress in unravelling Montgomery et al., 1994). It has been shown that the structure of variation in quantitative traits is litter size is genetically variable in outbred strains. It rather slow. The problem is that natural populations can be gradually increased or decreased by direct or are always under the strong influence of many random correlated selection. These findings have been inter- and systematic environmental effects. It is impossible preted as an indication of additive polygenic control # to control the environmental variables in the field and of this trait. However, the heritability (h ) of litter size therefore it is hard to assess the genetic architecture of was found to be very low. In laboratory and farm # the traits. animals studied so far h varied from 0 to 20% This problem can be solved in a laboratory (Falconer, 1989). This low heritability might result experiment. When we put representatives of natural from strong artificial selection for an increase in the populations in a controlled environment and breed litter size (that was applied for economic reasons in both livestock and laboratory animals). It may also reflect the consequence of strong natural selection that * Corresponding author. Institute of Cytology and Genetics SD RAS, 630090, Novosibirsk, Russia. e-mail: aks!bionet.nsc.ru has reduced an additive component of genetic varia- Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.126, on 24 Sep 2021 at 23:35:13, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0016672302005724 Yu. S. Aulchenko et al. 56 bility for litter size in the natural populations from were mated with 2 sires and 13 with 3 or more. In turn, which the founders of farm and laboratory animals the number of sires mated with 1, 2 and 3 or more came. dams was 42, 13 and 15, respectively. A study of heritability of this trait in animals that The other pedigree (Fig. 1b) originated from two were recently introduced into the laboratory and have parental couples. The founders were captured in the not been affected by selection in captivity may give us vicinity of Juiz de Fora, State Minas Gerais (21m58hS, a more accurate estimate of the genetic variability of 43m19hW) in 1994. Since then and until 1996 the litter size in natural populations. pedigree was maintained as an isolated stock at the Institute of Biology of the Federal University of Rio de Janeiro. A total of 32 sires and 31 dams in 38 2. Materials and methods parental couples produced 151 litters. In this pedigree only 7 dams were crossed with more than 1 sire while (i) Materials 6 sires were mated with more than one dam. Akodon cursor is a small rodent that is widely Both stocks were maintained in the same laboratory distributed in grassland areas of South America from conditions, under a natural daylight cycle. Litter size Central Brazil to Northern Argentina. The founders was scored at birth as the number of live-born of the captive-bred populations were isolated from offspring. The body mass of the dams was scored on natural populations of this species from Central– the day of delivery. Eastern Brazil. Both pedigrees contained multiple loops. Some of One pedigree (Fig. 1a) was established by crossing the loops were inbred. However, close inbreeding animals captured at Sumidouro, State Rio de Janeiro (crosses between relatives of the first degree) was rare: (22m03hS, 42m41hW) in 1989. Since then and until 1995 only 2 dams in the Sumidouro pedigree resulted from the stock was maintained at the Institute of Tropical such a cross and had an inbreeding coefficient 0n25. In Medicine (Rio de Janeiro). Additional founders were this pedigree there were 18 inbred dams participating captured during 1989–1993 at the same locality and in reproduction with an average coefficient of in- introduced into the pedigree. There were 34 founders breeding equal to 0n022. In the Juiz de Fora pedigree, and 115 non-founders involved in the crosses. A total despite a limited number of founders, there were only of 79 dams and 70 sires produced 171 litters. There 6 inbred dams with an average inbreeding coefficient were 50 dams that were mated with only 1 sire, 16 0n024. (a) (b) Fig. 1. Pedigrees of female grass mice Akodon cursor whose litter size was analysed. (a) Pedigree derived from founders captured at Sumidouro, State Rio de Janeiro. (b) Pedigree derived from founders captured at Juiz de Fora, State Minas Gerais. Open squares, male; open circles, female; filled circles, inbred female. There were 4 more females (not shown) that were introduced into the Sumidouro colony from the natural population at the final stage of colony formation. Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.126, on 24 Sep 2021 at 23:35:13, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0016672302005724 Inheritance of litter size in the Brazilian grass mouse 57 was expressed via parameters op , µ, A, D, τ , τ , τ , (ii) Segregation analysis # # q QQ Qq qq σG, σeq. We performed complex segregation analysis using a The estimates of genetic parameters were obtained mixed model of major-gene and polygene inheritance. using the maximum likelihood method (Kendall & Three mathematical components form the basis of Stewart, 1951). Hypotheses were tested by the like- complex segregation analysis: the penetrance function, lihood ratio test in a hierarchical manner. Twice the the gene frequency distribution and the transmission negative of the natural logarithm of the likelihood # probabilities distribution. The mixed model of in- ratio is asymptotically distributed as χ with degrees heritance assumes that a quantitative trait is under of freedom equal to the difference in number of control of a major gene, a large number of additive independent parameters of the two models under genetic factors and environmental factors (Morton & comparison (Neyman & Pearson, 1928). MacLean, 1974). The effects of these components To check the major-gene hypothesis we compared (major-genic, polygenic and environmental) are con- five genetic models: sidered to be independent of each other. Additional (1) sporadic model: the variation of the trait is covariates might be included in the model as in- assumed to be entirely due to non-genetic vari- dependent factors via regression. Thus, under the ation; mixed model the value of the quantitative trait y of i (2) polygene model: the major-gene component is some ith individual may be expressed as excluded; yi l µjµgijGijΣjbjxjijei, (3) mixed model: the transmission probabilities of the major gene are fixed at Mendelian values and all where µ is the general baseline mean, µ is the impact gi other parameters are estimated; from the major gene, G is the impact from the i (4) arbitrary transmission probabilities model: the polygenic component, e is the random effect of i least restricted model (all parameters are estimat- environment, x is the value of the jth covariate and ji ed); and b is the coefficient of regression of y on the jth j (5) equal transmission probabilities model: the re- covariate. striction τ l τ l τ is imposed on the model. It is assumed that the random environmental effects QQ Qq qq are distributed normally with mean zero and variance First, we tested for significance of genetic components # σe.

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