Behavioural Processes 108 (2014) 166–172

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Reduced mate preference for dominant over subordinate males in old female Syrian hamsters (Mesocricetus auratus) Ned J. Place a,∗ , Dianne M. Vernon a , Robert E. Johnston b a b

Department of Population Medicine & Diagnostic Sciences, Cornell University, Ithaca, NY 14853, USA Department of Psychology, Cornell University, Ithaca, NY 14853, USA

a r t i c l e

i n f o

Article history: Received 26 August 2014 Received in revised form 30 October 2014 Accepted 1 November 2014 Available online 7 November 2014 Keywords: Age Mating preference Hamster

a b s t r a c t Why some females choose to mate with a ‘preferred’ male, whereas others choose to mate with an ‘inferior’ male is not always clear. Generally, the choosiness of females is thought to decline with advanced age, but relatively few studies have investigated this concept, and reports of this phenomenon in mammals are lacking. To address this deficiency, young and old female golden hamsters were evaluated for their preference for dominant vs. subordinate males. Females observed male dyads as a dominance relationship was established. Dominant and subordinate males were then placed within enclosures at the opposite ends of a Y-maze, and the first approach, scent marking, and time spent near each male were evaluated in young and old females during pro-oestrus—a time when females solicit visits by prospective mates by leaving vaginal and flank scent marks. Whereas the proportion of time spent near the dominant male was significantly greater than random for both young and old females, the proportions of vaginal and flank scent marks left for the dominant male were significantly greater than random for young females, but not for old females. Overall, these results are consistent with a decline in the preference for dominant males by old female hamsters. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Under most circumstances life history theory predicts that old females should be less selective in choosing a mate than younger conspecifics (Kodric-Brown and Nicoletto, 2001; Ligout et al., 2012), because selection on traits that enhance fitness declines with age (Williams, 1957). Greater variation in mating preferences in old females as compared to young females is indicative of the age-associated relaxation of selection (Kodric-Brown and Nicoletto, 2001). Variation in mate selectivity can be influenced by extrinsic factors, e.g., predation risk (Magnhagen, 1991), or intrinsic factors, e.g., female reproductive quality (Moore and Moore, 2001). Parker (1983) suggested that choosiness is a function of female reproductive quality, an intrinsic factor that declines in many species as females age (Moore and Moore, 2001; Roff, 1992; Stearns, 1992). Therefore, selectivity for mates should also decline with age. Several reports have described this phenomenon in female insects, such as fruit flies, crickets, katydids, moths, and

∗ Corresponding author at: 240 Farrier Rd, Schurman Hall S1-088, Cornell University, Ithaca, NY 14953, USA. Tel.: +1 607 253 3796. E-mail addresses: [email protected] (N.J. Place), [email protected] (R.E. Johnston). http://dx.doi.org/10.1016/j.beproc.2014.11.002 0376-6357/© 2014 Elsevier B.V. All rights reserved.

cockroaches (Anjos-Duarte et al., 2011; Gray, 1999; Greenfield et al., 2004; Ligout et al., 2012; Moore and Moore, 2001), but the literature on reduced selectivity in older vertebrates appears to be far more limited, e.g., guppies and lizards (Kodric-Brown and Nicoletto, 2001; Richard et al., 2005). Interestingly, we found no studies reporting on the choosiness of female mammals as they age, especially as several mammals (e.g., mouse, Syrian hamster, rat, vole) have been shown to demonstrate female mate choice and a decline in fertility and fecundity as females age (Clutton-Brock and McAuliffe, 2009; Gosden et al., 1983; Huck et al., 1988; Merry and Holehan, 1979; Solomon and Vandenbergh, 1994). To determine if older female mammals are less choosy for prospective mates than younger conspecifics, we elected to study the golden Syrian hamster (Mesocricetus auratus). The preference that female hamsters have for dominant over subordinate males has been well established in this species (Brown et al., 1988; Huck et al., 1985; Lisk and Baron, 1983; White et al., 1986). The ageassociated decline in litter and weaning success in female Syrian hamsters has also been well documented (Huck et al., 1988). However, prior investigations of mating preference in female Syrian hamsters have involved relatively young females (3.6–6.0 months of age), and to our knowledge, the preference to mate with dominant males has not been investigated in older females. M. auratus is an excellent model for investigating the effects of aging on mate

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preference, because the majority of females maintain regular 4-day oestrous cycles into old age (Chen, 1981). This is critically important because tests for mate preference must be appropriately timed to the oestrous cycle. Thus, Syrian hamsters have a decided advantage over mice and rats, which have a high rate of irregular cycles, anoestrus, or persistent oestrus as they age (Finch et al., 1984). Lisk and Baron (1983) determined that females must interact with males prior to the onset of female receptivity in order for the dominant male to establish a clear mating priority. Therefore, pairs of young and old females observed pairs of dominant and subordinate males on the two days before pro-oestrus. On the day of pro-oestrus the young and old females were individually tested in a two-arm Y-maze with dominant and subordinate males held in a compartment at the end of each arm. Syrian hamsters leave vaginal scent marks during pro-oestrus to attract males prior to mating during oestrous on the following day (delBarco-Trillo et al., 2009a,b; Fischer and Brown, 1993; Lisk et al., 1983). Similarly, Huck et al. (1985) noted that females left more flank scent marks in the vicinity of the dominant male than the subordinate male. Therefore, we expected young females to leave the majority of vaginal and flank scent marks for the dominant male, and to spend more time in his company as compared to the subordinate male. Conversely, we expected old females to demonstrate reduced preference for the dominant male, which would be evident by old females dividing their scent marking and time near males more evenly between the dominant and subordinate males.

2. Methods 2.1. Animals Hamsters were born and maintained in captivity at Cornell University, Ithaca, NY, USA. Animals were weaned at 30 days of age and housed singly in polycarbonate cages (45 cm × 24 cm × 14.5 cm) with Sani-chip bedding; food (Prolab 1000, Syracuse, NY) and water were provided ad libitum. Hamsters were maintained in a 14-h light:10-h dark schedule with lights off between 9:00 and 19:00. All behavioural observations were made between 9:15 and 11:30 under dim and indirect light to facilitate direct observations and video recording. Home cages of experimental animals were kept in colony rooms that were used to house hamsters of both sexes, and experimental animals were transferred within their home cages to a nearby, separate room for behavioural testing. Experimental animals only occupied this room when testing was in progress; otherwise it was devoid of animals throughout the experiment. Eleven groups were evaluated, with each group consisting of four unrelated hamsters. Each group had a young and an old female and two adult males that were previously unfamiliar with the females and to one another. None of the animals had mated prior to this study. Mean ± SE ages of young and old females were 6.2 ± 0.3 and 14.9 ± 0.4 months, respectively. The age range was 4.6–7.5 months for young females and 13.1–17.4 months for old females. At these ages, Huck et al. (1988) reported that the reproductive success of old female hamsters was significantly reduced compared to young females. Because female Syrian hamsters prefer to mate with larger males (Drickamer et al., 1973), in the present study we matched pairs of adult males for body mass to within 5% of one another. Male dyads were also matched for age, with the mean difference within pairs being 1.9 ± 0.5 months. On the day before testing began, each pair of young and old females was confirmed to be in oestrus by placing a non-experimental tester male in their home cages and monitoring for lordosis—stereotypical arching of the back and raising of the tail. The same male was used for all oestrous tests and he was not allowed to mount the females. The regular 4-day oestrous cycle in Syrian hamsters (Lisk, 1985) assured

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that young and old females were matched for the day of the cycle throughout the behavioural testing, with days one through three of testing corresponding to metoestrus, dioestrus, and pro-oestrus, respectively. Experimental procedures were approved by Cornell University’s Institutional Animal Care and Use Committee (protocol #19930120) and conducted in accordance with the NRC Guide for the Care and Use of Laboratory Animals. 2.2. Behavioural tests and observations On day one of testing (metoestrus), the females were placed into enclosures that were at opposite ends of the males’ central arena. The females’ compartments (50 cm × 23 cm × 31 cm) were enclosed on all sides by clear plexiglas, save for the barrier that separated them from the males, which was a coarse wire mesh framed in plexiglas. Males were individually marked by gently affixing a small piece of green or yellow tape to the fur on their lower dorsum. Shortly thereafter the males were placed in the central arena (50 cm × 44 cm × 31 cm). They were initially covered with open-ended, clear plastic boxes to physically isolate them from the females and from one another until the start of the bout. The males were released simultaneously from the isolation boxes and monitored for 5 min by direct observations and video recording. Each male was returned to his home cage after the 5-min bout, and they were held there for 10 min. The females remained in their respective enclosures during the 10-min recess and during the second 5-min bout. Following the second bout the colored tape was removed from the males and all animals were returned to their home cages, which were returned to their usual colony rooms. The same steps were repeated on day two of testing (dioestrus). On day three of testing (pro-oestrus), the first bout followed the same steps as on the preceding days. After the first 5-min bout, all animals were returned to their home cages for a 10-min rest period. Thereafter, one of the females was placed in a Y-maze, which she was allowed to explore on her own for 5 min. The focal female had access to all areas of the Y-maze, save for the most distal regions of the two arms, which were used to individually confine the males behind a coarse mesh divider. All females investigated both arms of the Y-maze during their individual exploratory period. After the exploratory period, the focal female was moved into a small enclosure at the base of the maze and held there until the males were placed into the enclosures at the ends of the Y. The female was released from the base and monitored for 10 min by direct observations and video recording. The female and two males were returned to their home cages after the 10-min Y-maze test, and they remained there for 10 min until the next bout, which was identical in design to the first. During the 10 min between the first Y-maze test and the second bout and second Y-maze test, the Ymaze was cleaned with 50% ethanol. Another 10-min rest period followed the second bout, and the second female completed the Y-maze test thereafter, which followed the same design as the Ymaze test for the first female. After returning all four animals to their home cages and colony rooms, the Y-maze and bout arena were cleaned with 50% ethanol in preparation for the next group of four hamsters. No more than one group was ever tested over the course of a 3-day testing period. All females displayed lordosis on the day that followed day three of testing, confirming that all females had maintained a 4-day oestrous cycle and that day three coincided with pro-oestrus. 2.3. Scoring behaviour 2.3.1. Male arena bouts The dominant-subordinate relationship within each pair of males was determined by the consistent display of ‘tail-up’ by one

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of the males—the tail is raised and the back is arched upward whilst the male walks with a stiff-legged gait or freezes in position. The tail-up posture effectively reduces further attacks by the dominant male and reliably identifies the subordinate male (Johnston, 1985). Tail-up frequently follows the establishment of dominance through rolling fights, in which both males wrap themselves around one another, at which time they roll around whilst biting or attempting to bite each other in the flanks (Siegel, 1985). Bite injuries were rare, and when they did occur the wounds were superficial and the animals recovered from them quickly and completely. As the dominant male chases the subordinate male, the subordinate routinely runs away with his tail up. In the majority of the male dyads, the dominant-subordinate relationship was established on the first day during the first bout and maintained for the remainder of the bouts. However, in three groups the dominant-subordinate relationship reversed on day two, and then the relationship remained stable for the remainder of the bouts, and specifically for each of the bouts that immediately preceded the Y-maze tests. For each of the male bouts that preceded the Y-maze tests, we scored the video recordings for the time that the dominant male spent fighting, chasing and herding the subordinate male. We considered two events separate from each other when there was at least a delay of 4 s between them (delBarco-Trillo et al., 2009a,b). Fighting, chasing, and herding are aggressive behaviours that are listed in descending order of intensity, and we generated a composite ‘aggression score’ by summing the time spent displaying each behaviour after multiplying by an intensity factor—3× for fighting, 2× for chasing, and 1× for herding. For the first group of hamsters the dominant male was placed within the right arm of the Y for both the young and old females. For subsequent groups, the dominant male was alternately placed at the end of the left or right arm.

vaginal scent marks, flank scent marks and proximity times for each pro-oestrous female were calculated as proportions: (dominant−subordinate) (dominant+subordinate)

One group was excluded from the analysis of vaginal scent marks, because the old female for this group did not leave any vaginal scent marks, which would place a zero in the denominator of the calculation. Proportional data, which range from −1 to 1, were analyzed with the one-sample t-test or the non-parametric equivalent (Wilcoxon signed rank test) when the data were not normally distributed as determined by the Shapiro-Wilk test. This analysis was meant to determine if the preferences of the young and old females for dominant or subordinate males deviated significantly from random, which would have a value of zero (Morgan et al., 2011). A significant preference for the dominant male would have a strongly positive result, whereas a significant preference for the subordinate male would have a strongly negative outcome. Fisher’s exact test was used to evaluate numbers of young and old females that first approached the dominant or subordinate male and that spent the majority of time in close proximity to the dominant or subordinate male. To determine if female age or the magnitude of the dominant male’s aggressive behaviours in the bout arena influenced the focal female’s behaviours in the Y-maze we performed mixed model ANOVAs using female age and male aggression score as fixed effects. The interaction effect of female age and male aggression score was included in the model. Because each pair of young and old females was coupled with its own pair of dominant and subordinate males, group number (1–11) was included as a random effect in the model. Data are reported as means with standard errors, and differences were considered to be statistically significant at p < 0.05. 3. Results 3.1. Vaginal scent marks

2.4. Females in Y-maze Each female participated in a single Y-maze test on the day of pro-oestrus. The young female from the first group was the first to complete the Y-maze test, and for subsequent groups the first female tested alternated between old and young. The position of the females relative to the central bout arena also alternated between young and old on a group-by-group basis. Vaginal scent marking is a subtle behaviour that involves pressing the genital region against the substrate and moving forward (Johnston, 1985). Because vaginal scent marking can be difficult to detect on video recordings, the number and location of vaginal scent marks were recorded in real-time. The duration of time spent in close proximity to the dominant and subordinate males and the number of flank marks left by the females were scored from video recordings using EventCoder 1.0b11, a program written and kindly provided by Michael Goldstein (Cornell University, Ithaca, NY USA). During the Y-maze test, the focal female was considered to be in close proximity to a male if she was facing in his direction and her face and/or front paws were in contact with the mesh divider. The spacing of the wire mesh allowed the female and male to come into limited physical contact with one another, i.e., they could poke their noses through the mesh. The locations of vaginal and flank scent marks were scored as being within the right or left arm of the Y and then assigned to the dominant or subordinate male.

The proportion of vaginal scent marks that were left in the dominant male’s side of the Y-maze was significantly greater than random (zero) for young females (t = 4.30, p = 0.002), but not for old females (t = −1.34, p = 0.21; Fig. 1a). Female age had a significant effect on the proportion of vaginal scent marks left for the dominant male (F1,17 = 26.21, p = 0.002), but male aggression score did not (F1,17 = 0.53, p = 0.48), and there was no interaction effect of age and aggression score (F1,17 = 0.23, p = 0.61). Total number of vaginal scent marks left was not affected by female age (t = −0.04, p = 0.97; Fig. 1b). 3.2. Flank scent marks The proportion of flank scent marks that were left in the dominant male’s side of the Y-maze was significantly greater than random (zero) for young females (t = 3.80, p = 0.004), but not for old females (t = 1.84, p = 0.10; Fig. 2a). Female age and male aggression score did not have significant effects on the proportion of flank scent marks left for the dominant male (F1,19 = 0.45, p = 0.52; F1,19 = 0.24, p = 0.63, respectively), and there was no interaction effect of age and aggression score (F1,19 = 0.64, p = 0.43). Total number of flank scent marks left by young females was significantly greater than the number left by old females (t = 2.74, p = 0.01; Fig. 2b). 3.3. Time near males

2.5. Statistics Results were analyzed using a commercial statistical program (JMP version 10.0.2, SAS Institute, Cary, NC USA). The numberof

Seven of 11 (64%) young females first approached the dominant male and six of 11 (55%) old females first approached the dominant male (Fisher’s Exact test: p = 1.00). The proportions of time spent

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Fig. 1. (a) Proportion of vaginal scent marks left for the dominant male (mean + SE). *Denotes the proportion is significantly different than zero for young females. # Denotes the proportions for young and old females are significantly different. (b) Total number of vaginal scent marks (mean + SE) left by young and old females, with the number of marks left for the subordinate male (white bars) stacked upon the number of marks left for the dominant male (black bars).

near the dominant male were significantly greater than random (zero) for both young and old females (t = 4.16, p = 0.002 and t = 2.47, p = 0.03, respectively; Fig. 3a). Female age did not have a significant effect on the proportion of time spent near the dominant male (F1,19 = 3.59, p = 0.09), nor did male aggression score (F1,19 = 1.34, p = 0.26), and there was no interaction effect of age and aggression score (F1,19 = 0.92, p = 0.35). Total time spent near males did not substantially differ between young and old females (t = 0.13, p = 0.90; Fig. 3b). Ten of 11 (91%) young females spent the majority of ‘time near males’ with the dominant male and eight of 11 (73%) old females spent the majority of ‘time near males’ with the dominant male (Fisher’s Exact test: p = 0.59). 4. Discussion To our knowledge, this is the first report to show that female selectivity for the preferred class of males declines with age in

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Fig. 2. (a) Proportion of flank scent marks left for the dominant male (mean + SE). *Denotes the proportion is significantly different than zero for young females. (b) Total number of flank scent marks (mean + SE) left by young and old females, with the number of marks left for the subordinate male (white bars) stacked upon the number of marks left for the dominant male (black bars). ˆ Denotes the total number of flank marks left by young females is significantly greater than the number left by old females.

a species of mammal. Generally, variation in mate preference is expected to be greater in old than in young females (Kodric-Brown and Nicoletto, 2001), and our results are fundamentally consistent with that prediction. The cost-benefit trade-offs of being choosy are likely to change as females age, owing to the age-associated decline in reproductive quality (Moore and Moore, 2001; Parker, 1983). Huck et al. (1988) reported that reproductive quality was significantly reduced in 15-month-old hamsters as compared to 6-month-old females, and the findings of the present study are consistent with reduced selectivity in the old cohort of females. Young female Syrian hamsters consistently demonstrated a preference for the dominant male by spending proportionally more time near him and by leaving proportionally more flank and vaginal scent marks within his side of the Y-maze. Conversely, even though old females spent proportionally more time near the dominant male, the allocation of vaginal and flank scent marks left by old females did not differ significantly from random. Male

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Fig. 3. (a) Proportion of time spent near the dominant male (mean + SE). *Denotes the proportions of time spent near the dominant male are significantly different than zero for young and old females. (b) Total time (s) spent near males (mean + SE) by young and old females, with the time for the subordinate male (white bars) stacked upon the time for the dominant male (black bars).

hamsters are attracted to and excited by vaginal secretions (Johnston, 1974, 1975), and females leave vaginal scent marks on the day of pro-oestrus to attract males to their burrow in preparation for mating on the following day of oestrus (delBarco-Trillo et al., 2009a,b; Fischer and Brown, 1993; Huck et al., 1985). In previous studies involving the mating preferences of young female hamsters, when females had direct access to tethered or freely roaming males, vaginal and flank scent marks were decidedly in favor of the dominant male, as were the mating opportunities (Huck et al., 1986). Whereas we found that the proportion of vaginal and flank scent marks left by old females did not favor the dominant male (Figs. 1a and 2a), it remains to be determined if actual mating preference for the dominant male is reduced in old females when they have direct and equal access to dominant and subordinate males. Interestingly, similar to young females, old females spent significantly more time near the dominant male than near the subordinate male, and yet old females did not leave a greater number or

proportion of vaginal or flank scent marks for the dominant male. Reduced sensory perception in older females might be a proximate explanation for the reduced scent marking in the vicinity of the dominant male relative to the time spent near him. Female hamsters could use multimodal signals (e.g., olfactory, auditory, and visual) to perceive differences between dominant and subordinate males (Ronald et al., 2012), and an age-associated decline in sensory perception could reduce the discriminatory abilities of old females. Olfaction is a possible mode of perception that female hamsters use to assess male status. The flank gland is larger and more pigmented in dominant than in subordinate males (Drickamer et al., 1973), and in studies involving 4-months-old females, the scent gland secretions from dominant males were preferred over subordinate males (Montgomery et al., 1988). White et al. (1986) also found that female hamsters preferred the urine odor cues from dominant males over subordinate males. Odor perception decreases with aging in women (Doty et al., 1984; Doty, 2009; Murphy et al., 2002), but whether aging adversely affects hamster olfaction remains to be studied. In addition to olfaction, female hamsters might also be able to distinguish dominant males from subordinate males through sight. However, visual perception might also decline with age in female hamsters. Body size is a likely visual cue in hamsters, as females prefer to mate with larger males (Drickamer et al., 1973), but we controlled for this variable by matching the male dyads to body mass. Another possible visual cue is the stripe that ornaments the chest region of hamsters, however, female hamsters have not been found to demonstrate a preference for any particular pattern (Johnston, 1976). The ability to process auditory stimuli has been shown to decline with age in gerbils (Boettcher et al., 1993) and in rats (Parthasarathy and Bartlett, 2011), and the same might be true in hamsters. Johnston and Kwan (1984) found that vaginal scent marks elicited ultrasonic courtship calling in males, but we know of no reports of females preferring the ultrasonic calls of dominant males. If ultrasonic calls prove to be a cue that female hamsters use in mate selection, then an age-related decline in auditory processing could contribute to a reduced ability to distinguish between dominant and subordinate males. Hormones also modulate auditory processing in mammals (Al-Mana et al., 2010; Miranda and Liu, 2009), and it is conceivable that hormonal profiles differed in young and old hamsters, even though both age classes were cycling regularly and were tested on the same day of the oestrous cycle. Saidapur and Greenwald (1978) noted substantial variation in sex steroid concentrations during pro-oestrus in adult hamsters (presumably young), and future studies comparing the mating preferences of young and old hamsters should include assessments of hormones and receptors that are known to modulate auditory processing (e.g., oestradiol). The levels of male-male aggression during the bouts that immediately preceded the Y-maze tests were highly variable within and among the 11 groups (Fig. 4). For some groups the level of aggression between males was more intense during the first bout than during the second, and for others the order was reversed or the two bouts were similar in aggression intensity. Based on the concepts of value-sensitive decision-making (Pais et al., 2013), we hypothesized that old females might require a greater minimum difference between the dominant and subordinate males for discrimination purposes. However, the intensity of aggression, as reflected in the composite aggression scores, did not appear to have a significant impact on female behaviours in the Y-maze. Because there are no clear rules of engagement, it is difficult to score a bout between male hamsters like a boxing match, and more importantly it is difficult to determine which factors weigh most heavily in a female’s decision. Within the Y-maze, all females paid multiple visits to the dominant and subordinate males, but we were unable to identify any obvious cues that might have influenced female scent marking

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References

Fig. 4. Aggression scores for pairs of males in groups 1–11 during the first and second arena bouts that immediately preceded the Y-maze tests on the females’ day of prooestrus. The times that the dominant male spent fighting with, chasing and herding the subordinate male were weighted according to their intensity to generate the aggression scores ([fighting × 3] + [chasing × 2] + [herding × 1]).

behaviour. Male olfactory, visual and auditory cues could potentially be manipulated or negated (e.g., scent gland removal, muting) in future studies in order to determine which male signals are most informative. Collectively, the present study provides evidence for the first time that female mate preference declines with age in a mammal. Several potential mechanistic explanations exist, not least of which is the possibility that old females have experienced a decline in sensory perception in one or more relevant modalities. This is a testable hypothesis that warrants further study. Because the rate of decline in sensory perception is likely to vary among individual females as they age (Collier and Coleman, 1991), some old females may retain good sensory perception, and thus remain selective in their preference for mates. However, given the right circumstances an old female with poor sensory perception could still display strong mate preference if she is provided with an opportunity to choose from males whose qualities are easily distinguishable. The ageassociated decline in reproductive quality that is characteristic of female mammals has the potential to generate increased variation in selectivity between and within individual females, and this phenomenon can be exploited as a tool to explain individual differences in the expression of behaviours associated with mate choice. Studies are ongoing to determine if chronologically age-matched female hamsters that differ in their reproductive quality (e.g., size of the ovarian reserve of oocytes) demonstrate predictable differences in their preference for mates. If an individual female’s residual reproductive value influences her selectivity for mates, then we would predict that an old female of relatively high reproductive quality for her age would maintain selectivity for the preferred class of males.

Acknowledgements We thank Marcela Fernandez-Vargas and Joan Johnston for advice in working with golden Syrian hamsters, Jay Barry for advice on the statistical analysis, Elliott Place for scoring behaviour videos, David Peck, Kristen Roosa, and three anonymous reviewers for their comments on an earlier draft, and the Cornell Center for Animal Resources and Education for excellent animal care.

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