A comparative study of parental care between two rodent species: implications for the mating system of the mound-building mouse Mus spicilegus
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.
References (45)
Oestrous female house mice discriminate dominant from subordinate males and sons of dominant from sons of subordinate male by odour cues
Anim. Behav.
(1992)Contributions of paternal care in the growth and development of the young in Peromyscus californicus
Behav. Biol.
(1974)Mating systems, philopatry and dispersal in birds and mammals
Anim. Behav.
(1980)Fitness effects of communal rearing in house mice: the role of relatedness versus familiarity
Anim. Behav.
(1994)- et al.
A comparison of maternal behavior in the meadow vole (Microtus pennsylvaticus), prairie vole (Microtus ochrogaster) and pine vole (Microtus pinetorum)
Anim. Behav.
(1984) - et al.
Monogamy and long-term pair-bonding in vertebrates
Trends Ecol. Evol.
(1990) - et al.
A comparison of paternal behaviour in the meadow vole Microtus pennsylvaticus, the pine vole M. pinetorum and the prairie vole M. ochrogaster
Anim. Behav.
(1986) The ecology of territoriality in small mammals
Trends Ecol. Evol.
(1990)- et al.
Female sexual preferences differ in Mus spicilegus and Mus musculus domesticus: the role of familiarization and sexual experience
Anim. Behav.
(1998) - et al.
Biochemical diversity and evolution in the genus Mus
Biochemical Genetics
(1984)
The reproductive ecology of the house mouse
Q. Rev. Biol.
Monogamy and the prairie vole
Scientific American
Mammalian mating systems
Proc. R. Soc. Lond.
The Evolution of Parental Care
Parental investment
Social organisation and territorial behaviour in the wild house mouse (Mus musculus L.)
Proc. Z. Soc. Lond.
Mating systems
An exercise in the prediction of monogamy in the field from laboratory data on 42 species of muroid rodents
The Biologist
Paternal behavior in rodents
Am. Zool.
Cited by (59)
Transmission of food preference via faeces in male and female house mice: Who is a good provider of food cues?
2020, Behavioural ProcessesCitation Excerpt :Mound-building mice and house mice are closely related species but differ greatly in their socio-spatial organization. The paternal behaviour displayed by mound-building mouse males contributes efficiently to the reproductive success of a female and mate selection is a key factor of female reproductive success (Patris & Baudoin, 2000; Gouat & Féron, 2005; Féron & Gouat, 2007). Our results suggested that, contrary to females, males prioritized the information relative to a novel potential sexual partner, i.e. unfamiliar female, rather than food-related information.
Timing of reproduction and paternal cares in the crested porcupine
2016, Mammalian BiologySimilarity of personalities speeds up reproduction in pairs of a monogamous rodent
2015, Animal BehaviourMaternal energetic investment in a monogamous mouse
2014, Mammalian Biology