A comparative study of parental care between two rodent species: implications for the mating system of the mound-building mouse Mus spicilegus

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Abstract

Paternal care is uncommon in mammals where males are more often involved in sexual competition than in providing care for their own offspring. However some species present some form of paternal care and, most of the time, this phenomenon is associated with a monogamous mating system. Mice of the genus Mus, such as the house mouse Mus musculus domesticus, are commonly considered to be polygamous–polygynous species. In Mus spicilegus, the mound-building mouse, previous results on female sexual preferences have suggested the existence of pair bonding more compatible with a monogamous mating system than with a polygamous one. We therefore tested the hypothesis that male M. spicilegus present a higher level of paternal care than males of the polygynous house mouse. Results showed that male M. spicilegus spent significantly more time covering the young during the first week after birth than male M. m. domesticus, particularly when the female was exploring, and retrieved stray pups significantly more frequently and more rapidly than male M. m. domesticus. There were practically no differences between the females of these two species. M. spicilegus parents also more significantly alternated their protection of the pups than M. m. domesticus parents. We discuss the evolution of paternal care in M. spicilegus in relation to monogamy.

Introduction

The observed variation in mating systems among mammals is considered to result mainly from differences in female dispersion and male capacity to monopolize several females (Wittenberger, 1980, Clutton-Brock, 1989, Komers and Brotherton, 1997, Favre et al., 1997). Mating systems include a description of how mates are acquired, their number, the characteristics of pair bonding, and patterns of parental care by each sex (Emlen and Oring 1977). Most mammal species are polygynous (Kleiman, 1977), with male investment being limited to fertilization, whereas females, through gestation and lactation, invest heavily in the offspring's survival (Trivers, 1972). In such species, reproductive success is limited in females by their access to resources and in males by their access to females (Trivers, 1972, Vehrencamp and Bradbury, 1984, Davies, 1991). However in some species, reduced opportunities for males to gain control of more than one female can lead to a monogamous mating system involving some form of paternal care (Kleiman, 1977, Wittenberger and Tilson, 1980).

Parental care corresponds to any form of parental behaviour which appears likely to increase the fitness of a parent's offspring but also the reproductive success of parents (Trivers, 1972, Clutton-Brock and Godfray, 1991). Some authors (Kleiman and Malcolm, 1981, Elwood, 1983) distinguish direct parental behaviour when the pups are present (thermic protection, huddling with young, feeding, licking, retrieving) and indirect parental behaviour which can occur without the presence of the pups (provision of food, protection from predators or members of own species, nest building). Others (see review in Clutton-Brock, 1991) propose to distinguish “depreciable” parental care, such as the provision of food, where investment is correlated to brood size, and “nondepreciable” care such as parental vigilance where investment is not correlated to brood size.

Phylogenetic data have revealed the existence of several species of the genus Mus in Europe, including Mus musculus domesticus, the house mouse and Mus spicilegus, the mound-building mouse (Bonhomme et al., 1984, Boursot et al., 1993). The house mouse is characterized by a polygamous–polygynous mating system, which results from a dominance–submission relationship between males inside the social group (Crowcroft and Rowe, 1963, Reimer and Petras, 1967, Lidicker, 1976, Bronson, 1979, Gerlach, 1990) and female sexual preferences for dominant males (Drickamer, 1992). M. spicilegus, a mouse of eastern Europe, is mainly characterized by the autumnal building of mounds (with stock of seeds) where mice stay during the winter without reproducing (Naumov, 1940, Pisareva, 1948, Festetics, 1961, Murariu, 1981, Orsini et al., 1983, Duryadi, 1993). The mating system of the species remains poorly documented, although genetic analyses have shown that young found in the mounds at the end of the autumn originated from several unrelated males and several related females (Garza et al., 1997). Another recent study (Milishnikov et al., 1998) concludes that the genetic variability in mound-building mice populations is relatively low and indicates annual variations of the sex ratio which is biased in favor of females during the summer. A previous behavioural study (Patris and Baudoin, 1998) showed that M. spicilegus females present a sexual preference for their familiar mate during the breeding season and generally refuse to copulate with an unfamiliar one, whereas the reverse is observed in M. m. domesticus. This result is highly suggestive of a strong pair bonding in M. spicilegus and the possibility of a monogamous mating system, as observed in other monogamous rodent species (Mock and Fujioka, 1990, Carter and Getz, 1993).

In laboratory conditions, male house mice present some form of paternal behaviour (Dewsbury, 1981), as observed in males of several rodent species (Elwood, 1983, Dewsbury, 1985). However, males of monogamous rodent species display significantly more paternal care than males of polygynous ones (McGuire and Novak, 1984, McGuire and Novak, 1986, Oliveras and Novak, 1986). Therefore we compared parental and particularly paternal care between M. spicilegus and M. m. domesticus and tested the hypothesis of a higher level of paternal care in the supposedly monogamous M. spicilegus. Parental behaviour can be measured at three different levels: its form, frequency or duration; the parent's expenditure of energy on caring for its offspring; and the cost of parental care to the parents' future fitness or residual reproductive value (Clutton-Brock and Godfray, 1991). As a parent's expenditure of energy is difficult to correlate with a mating system under standard laboratory conditions, we restricted our study to the characteristics and particularly the duration of paternal and maternal care as indications of parental motivation. The first part of this work examines the proportion of paternal and maternal time spent in covering the young during the first week after litter birth, when pups are thermic dependant, as a criteria of parental care investment (Kleiman and Malcolm, 1981). The second part examines pup retrieval behaviour by males and females, as an indication of responsiveness toward the young (Dudley, 1974, Elwood, 1983).

Section snippets

Animals and breeding conditions

The M. m. domesticus and M. spicilegus mice used in this study were derived from stocks caught in the wild and reared in captivity for 15 generations. The original stocks were trapped by Dr Bonhomme's team (CNRS UPR 9060, Montpellier, France): M. spicilegus, strain ZYP (Pancevo, Yougoslavie); M. m. domesticus, strain DDO (Odis, Denmark). The mice were maintained in the laboratory under a 14:10 h light:dark cycle, with an ambient temperature of 20±2°C in both the breeding and the experimental

Night period

The analysis of the seven nights after birth shows that M. spicilegus pups were significantly more covered by their parents than M. m. domesticus pups (Fig. 1: F1.14=15.17, P<0.01). Male M. spicilegus spent significantly more time covering the young over the seven nights than male M. m. domesticus (F1.14=10.22, P<0.01) with a significant “species×days” effect (F6.84=3.4, P<0.01), where M. spicilegus males progressively increased the time spent in covering the pups while the reverse was observed

Discussion

Male M. spicilegus spent more time covering pups than male M. m. domesticus, during both night and daylight periods, whereas no difference was found between females except during the first daylight period after delivery. As females of these two species did not display any aggressive behaviour toward their partner, the interspecific differences observed between males could correspond to a higher paternal motivation in M. spicilegus toward their pups. In addition, M. spicilegus partners

Acknowledgements

We would like to thank François Bonhomme and Annie Orth for providing the two species of mice. We are grateful to Simone Demouron for her help in taking care of the animals. We would also like to thank P. Gouat for his statistical advice, Gilles Gheuzi and Christophe Féron for discussions, Sevane Maslak and Andrea Dejean for the revision of the English version of the manuscript, and Lesya Vynogradska for the translation of articles from Russian.

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