Male-female associations and female olfactory neurogenesis with pair bonding in Mus spicilegus

Abstract

Mound-building mice Mus spicilegus exhibit life-history traits that are unique among the Mus species complex, such as the cooperative mound-building behaviour that gives the species its common name. In this and other socially coordinated activities, such as those associated with reproduction, these mice should be able to recognize individuals (via discrimination based on kinship, population and species) to mediate their interactions. Our previous studies have provided evidence of population and species recognition in M. spicilegus . The aims of the present study were: (i) to study associations of mice during their reproductive period (in outdoor enclosures), (ii) to investigate whether there is an influence of relatedness of females in these associations, (iii) to determine whether female M. spicilegus are able to make kin vs. non-kin discriminations, and (iv) to study certain neurobiological correlates of male-female bonds. Stable male-female associations were found in almost all the experimental groups, both those with unrelated and unfamiliar females and those with unfamiliar sisters. Kinship between females did not affect female associations in our enclosure experiment, but in our kin discrimination experiment females did distinguish between unfamiliar sisters and unfamiliar unrelated females. Shared kinship may not encourage cooperative rearing of pups but could enhance cooperation in building mounds where mice over-winter. Male-female associations could be based on a social bond, as hypothesized from previous laboratory experiments. This was substantiated in this study by increased olfactory bulbar neurogenesis in females that preferred (in two choice tests) their sexual partner 3 weeks after their first mating. Based on these results there is clear evidence to suggest that the mating system of M. spicilegus is social monogamy.

Social regulation of adult neurogenesis in a eusocial mammal

“…In line with prior research indicating that social factors, such as mating experience and opposite-sex chemosensory cues affect olfactory neurogenesis in adulthood (Smith et al, 2001;Baudoin et al, 2005;Mak et al, 2007;Larsen et al, 2008;Oboti et al, 2009;Corona et al, 2011), DCX expression in layer II of the PCx was highest in subordinates that were removed from their natal colonies and paired with an unfamiliar, opposite-sex conspecific. This is the first study to date to examine the relative contributions of mating experience and opposite-sex social/chemosensory stimulation to neurogenesis in the PCx; our results suggest that neurogenesis in this region is predominantly regulated by chemosensory exposure.…”

“…One line of research highlights how distinct aspects of social life (E.g., sexual encounters, gestation, parenthood, and chemosensory cues conveying the sex, status and health of conspecifics) regulate the birth, fate, and integration of adult-born neurons. For example, mating encounters or exposure to opposite-sex chemosensory cues up-regulate cell proliferation in the rodent DG and SVZ (Smith et al, 2001;Larsen et al, 2008;, as well as the survival and differentiation of newborn neurons in the DG and olfactory bulb (OB) (Baudoin et al, 2005;Mak et al, 2007;Larsen et al, 2008;Oboti et al, 2009;Corona et al, 2011).…”

Comparison of Urinary Scents of Two Related Mouse Species, Mus spicilegus and Mus domesticus

“…In this species, social and kin recognition through olfactory cues have been observed in several studies (Gouat et al, 1998;Dobson and Baudoin, 2002;Baudoin et al, 2005;Busquet and Baudoin, 2005;Todrank et al, 2005;Colombelli-Negrel and Gouat, 2006). The major mammalian scent sources for chemical communication are sex glands, other skin glands or urine.…”

“…Unlike M. domesticus, M. spicilegus are monogamous (Patris and Baudoin, 1998;Dobson and Baudoin, 2002;Baudoin et al, 2005;Gouat and Féron, 2005) and build co-operatively colonial mounds for overwintering (Orsini et al, 1983;Garza et al, 1997;Poteaux et al, 2008). Moreover, M. spicilegus males display intense paternal care (Patris and Baudoin, 2000;Féron and Gouat, 2007).…”

Sex-Specific Modulation of Cell Proliferation by Socially Relevant Stimuli in the Adult Green Treefrog Brain <i>(Hyla cinerea)</i>

“…The reception of social stimuli has been shown to modulate adult neurogenesis (or cell proliferation) in specialized nuclei related to signal production, such as the prepacemaker nucleus of electric fish [Dunlap et al, 2006] and song control nuclei of songbirds [e.g., Lipkind et al, 2002;Barnea et al, 2006], and in the olfactory system of mammals [e.g., Smith et al, 2001;Fowler et al, 2002;Baudoin et al, 2005], for which pheromone signals are important. It remains to be seen whether social stimulation influences cell proliferation in more integrative areas of the social brain that are less strictly tied to motor pattern generation or sensory reception, such as the preoptic area (POA) and caudal/ventral hypothalamus.…”