Asynchronous breeding in the socially monogamous prairie vole.(Report)

Abstract: At least two hypotheses have been proposed for why animals should breed synchronously: (1) to swamp predators and reduce the probability of offspring being killed and (2) to promote monogamy when paternal care is important for offspring survival. Thus prey and monogamous species are likely candidates for synchronous breeding. We conducted an experiment to determine if a prey species, the monogamously breeding prairie vole (Microtus ochrogaster (Wagner, 1842)), breeds synchronously. We conducted eight replicates in which we placed six nulliparous females and six adult males in semi-natural enclosures for 18-21 days to determine if they bred synchronously. The time of conception ranged from 2 to 18 days within replicates with no indication of breeding synchrony within any of the populations. Thus neither predator avoidance nor paternal care models were supported for prairie voles. We conclude that rodents in general are not good models for breeding synchrony and that females use alternative mating tactics to enhance their lifetime reproductive success. We discuss our results in the context of the prairie vole mating system.

Resume : Au moins deux hypotheses existent pour expliquer pourquoi les animaux devraient se reproduire en synchronie : (1) soit pour saturer les predateurs et reduire ainsi la probabilite de mort des rejetons et (2) soit pour promouvoir la monogamie lorsque les soins parentaux sont importants pour la survie des petits. C'est pourquoi les proies et les especes monogames sont plus susceptibles d'avoir une reproduction synchronisee. Nous avons mene une experience pour determiner si une espece proie, le campagnol des prairies (Microtus ochrogaster (Wagner, 1842)), a reproduction monogame, possede aussi une reproduction synchronisee. Nous avons etabli huit experiences reiterees dans lesquelles nous avons place six femelles nullipares et six males adultes dans des enclos semi-naturels pendant 18-21 jours pour voir s'ils se reproduisaient de facon synchronisee. Le moment de la conception variait de 2 a 18 jours dans les experiences reiterees et il n'y a d'indication de synchronie de la reproduction dans aucune des populations. Ainsi, ni le modele d'evitement des predateurs, ni celui des soins parentaux ne s'appliquent chez ces campagnols des prairies. Nous en concluons que les rongeurs ne constituent pas en general de bons modeles pour la synchronie de la reproduction et que les femelles utilisent des tactiques d'appariement de rechange pour augmenter leur succes reproductif sur l'ensemble de leur vie. Nous discutons de nos resultants en regard du systeme d'appariement des campagnols des prairies.

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Introduction

Theoretical explanations have been presented for the adaptive significance, or at least the functional consequences, of synchronous and asynchronous breeding in animals. Breeding synchrony has been proposed as an adaptive mechanism to satiate predators by producing many young at one time. In this case, offspring survival is a function of the probability of being detected and caught. Supportive evidence for this hypothesis occurs in a number of species including prairie dogs (genus Cynomys Rafinesque, 1817; Hoogland 1981), American bison (Bison bison (L., 1758); Wolff 1998), the marsupial Antechinus stuartii Macleay, 1841 (Scott 1986), and numerous species of large herding ungulates (e.g., Rutberg 1987; Sinclair et al. 2000). Whereas breeding synchrony may be adaptive when young are conspicuous and vulnerable, breeding asynchrony may be favored when young are widely dispersed or hidden from predators, as occurs in smaller isolated herbivores such as gazelles (genus Gazella Blainville, 1816) and impala (Aepyceros melampus (Lichenstein, 1812); Sinclair et al. 2000). Among small rodents, breeding synchrony may be adaptive under some circumstances (e.g., Ims 1987; Ims et al. 1988); however, reproductive synchrony can be maladaptive if generalist predators exhibit short-term functional and numerical responses to prey availability (Ims 1990). The one study to examine timing of breeding in a small fossorial rodent showed no evidence of synchrony (Ims et al. 1988).

A second hypothesis for synchronous breeding is for females to monopolize dominant or paternal males. If a female can benefit by keeping one male to herself, such as to provide paternal care beyond conception, synchronous estrus decreases the chances that males will be polygynous or have time for philandering (Emlen and Oring 1977). This female strategy might force males to invest more time and energy on parental care in that additional sexually receptive females are not available (Knowlton 1979). Some data exist to support this hypothesis (e.g., Ethiopian wolves, Canis simensis Ruppell, 1840 (Sillero-Zubiri et al. 1998); feral cats, Felis catus L., 1758 (Say et al. 2001)). In contrast, if paternal care is not needed, asynchronous estrus might be adaptive for females in that it provides them with a greater pool of males from which to select a mate. Thus sexual selection should be more pronounced in species that mate asynchronously than synchronously (Emlen and Oring 1977). Ims (1987) further proposed that synchronous breeding should produce a monogamous mating system, whereas if females are asynchronous males could wander and mate promiscuously.

The objective of this study was to test whether prairie voles (Microtus ochrogaster (Wagner, 1842)) fit the predictions of these models. Prairie voles are socially monogamous (Getz et al. 1981, 1993; Carter and Getz 1993; Ophir et al. 2008) and males provide extensive parental care (e.g., Thomas and Birney 1979; Oliveras and Novak 1986). Females and males form pair bonds and share the same homerange space (Hofmann et al. 1984). According to the Emlen and Oring (1977) model, monogamy should be associated with synchronous breeding. If breeding is asynchronous, males and females may be pursuing alternative reproductive tactics to monogamy (e.g., Wolff 2008), or further explanations may be needed to evaluate the association between timing of breeding among females and mating system.

Materials and methods

The data provided in this study were collected in part from another study in which we assessed space use, mating behavior, and reproductive success of male and female prairie voles in outdoor semi-natural enclosures (Ophir et al. 2007, 2008). A trial consisted of placing six males and six females into an enclosure for 18-21 days. At the end of a trial all animals were removed and euthanized so that we could determine the stage of pregnancy. We conducted eight trials, with four trials composed of voles from Illinois (IL) and four with voles from Tennessee (TN). All individuals were first, second, or third generation offspring, derived from outbred wild-caught populations from Shelby County, Tennessee (near Memphis: 35[degrees]07'N, 89[degrees]58'W), or Champaign County, Illinois (near Urbana: 40[degrees]6'N, 88[degrees]12'W). Animals in each trial were sexually mature; all females were nulliparous. All animals were released into a 0.1 ha enclosure planted with natural vegetation (details of facility are provided in Mahady and Wolff 2002). We ear-tagged and weighed all individuals before introduction to field enclosures and standardized groups for age and body mass. Two replicate trials were conducted simultaneously, one with voles from each geographical region. The behavior of individuals from these two populations does not differ in any biologically identifiable way (Ophir et al. 2007), consequently the trials were considered eight replicates. The details on parentage and space use are provided in Ophir et al. (2008).

Trials were conducted from July to October 2004. We trapped and removed animals from day 18 to day 21, to allow enough time for fertilization to have occurred but before parturition (gestation is ~21 days). All animals were trapped and removed from enclosures before any births occurred. Females were euthanized and we measured the crown-rump length of embryos as an indication of date of conception. For prairie voles, each millimetre of length is about equal to 1 day of growth (21 mm is 21 days of gestation and size at birth; J. Wolff and S. Thomas, unpublished data).

Estimating synchrony

To estimate the index of reproductive synchrony (I), we followed the procedure of Ims et al. (1988). We calculated the pairwise differences in the date of conception between females within a population and then squared each pairwise difference. In a synchronously breeding population, the dates of conception within an estrus cycle coincide and the mean of these pairwise contrasts approaches zero. At the other extreme, a population in which females are maximizing the spacing of conception will be equally likely to breed at any date, and this will produce large differences between conception dates in females.

In our study, we first estimated the degree of active synchrony by calculating the pairwise contrasts between females within an enclosure. We defined date of conception relative to the date females were introduced into the enclosure. Females in different enclosures could not interact with one another; we thus considered the differences in conception dates between females in different enclosures to form a null expectation for the distribution of Ims et al. (1988) synchrony statistic. We compared the pairwise contrasts for females within an enclosure to the contrasts of females in different enclosures using a Mann-Whitney U test. If females within an enclosure were breeding synchronously, the mean pairwise contrast should be less than it is between females housed in separate enclosures. If females were spacing their breeding, the within enclosure contrasts should be greater than the between enclosure contrasts. Lastly, if females are breeding independently of one another, within and between enclosure contrasts should be similar.

Results

Across all eight separate experimental populations, 30 of the 48 females were pregnant at the time of trapping. The time of conception for the 30 pregnant females ranged from 2 to 18 days. The remaining 18 females either did not breed or died before the end of the experiment. In only one TN enclosure did two females conceive on the same day; in all other cases only one female bred on any given day (Fig. 1).

The index of reproductive synchrony (I) was 80.38 [+ or -] 12.02 (mean [+ or -] SE; Ims et al. 1988). If female prairie voles bred synchronously, I (the contrasts between pairs for the timing of insemination within an enclosure) should be less than the null distribution (contrasts between females in different enclosures; null = 65.62 [+ or -] 3.87). Our data demonstrated that the distribution characterizing timing of female insemination (I) was no different from the null expectation of asynchronous breeding (Mann Whitney U test, U = 7545.5, [N.sub.within enclosure] = 45, [N.sub.between enclosure] = 390, P = 0.12; Fig. 2). If a tendency for I to differ from the null existed, it was in the opposite direction than would be predicted for synchronous breeding, suggesting that our sample of females bred more asynchronously than expected by chance.

Discussion

Our results do not support synchronous breeding in prairie voles. The timing of breeding for females under experimental field conditions indicates that no intrinsic social cues were used to synchronize breeding. The data suggest that breeding was not synchronized in eight individual populations and collectively did not deviate from random, ranging from 0 to 18 days in all 30 females over a 21-day period (Fig. 1). Considerable evidence is available from laboratory and observational studies showing that pheromones and other chemical signals can either stimulate or inhibit reproduction in other females (e.g., Handelmann et al. 1980; Dluzen et al. 1981; Scott 1986; Wolff 1998; reviewed in Drickamer 2007). However, under the conditions of this study, we had no indication that females in each of eight populations synchronized their breeding. A similar lack of breeding synchrony was found for several populations of Norwegian lemmings, Myopus schisticolor (Lilljeborg, 1844) (Ims et al. 1988).

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[FIGURE 2 OMITTED]

Our results support the arguments of Ims (1990) that predation is insufficient to select for breeding synchrony in prairie voles or perhaps other small secretive fossorial rodents (see also Ims et al. 1988). Predators of these small rodents are opportunistic and do not appear to specialize on young individuals, especially considering that they are confined to underground burrows until independence. A similar argument was presented by Sinclair et al. (2000) for ungulates in that isolated individuals or small groups of herbivores that hide their young tend to breed asynchronously.

Our results also are inconsistent with the Emlen and Oring (1977) model that predicts asynchronous breeding should result in wandering promiscuous males. In this study, 74% of males formed pair bonds and were socially monogamous for the duration of the trial (Ophir et al. 2008). Thus, the tendency for males to consort with just one female was not a function of timing of reproduction. Paired males were just as likely to remain with their paired females whether they were impregnated the first day of the trial or did not breed at all. Only 11 of 43 males were considered wanderers in this study in that they did not remain on a given female's territory. Each of four paired females that never bred in this study had a permanent resident male on their territories that was never observed away from the female's territory. Thus, social monogamy was independent of timing of estrus or availability of neighboring estrous females.

Numerous studies with prairie voles, including this one, indicate that males are socially monogamous and remain committed to one female (e.g., Getz et al. 1981, 1993; Wang et al. 1998; Young et al. 1998; Ophir et al. 2008). These studies, however, have been conducted over short time periods or in the laboratory even under shorter time periods, often less than 10 days. Prairie vole males do provide parental care (e.g., Thomas and Birney 1979; Oliveras and Novak 1986). However, females do not necessarily stay with one male through successive pregnancies; rather, they switch partners and become serially monogamous or in some cases mate with multiple males (Solomon et al. 2004; Ophir et al. 2008; S. Thomas, personal communication (2008); N. Solomon, personal communication (2008)). Consequently, asynchronous mating may actually be adaptive for females in that it gives them opportunities to seek new mates after each litter. If males mate-guard primarily during the 6-8 h period of postpartum estrus and remain socially monogamous for the remainder of gestation, they would still be available for mating with neighboring females. Because of high levels of asynchronous breeding in our study, 4-5 of the 6 males in each enclosure would be available for mating with other females at any given time. Thus asynchronous breeding provides a greater opportunity for switching partners or at least for extra-pair copulations. We suggest that mate-guarding and social monogamy may be a male tactic to ensure some reproductive success (e.g., Hodges et al. 2002; Ophir et al. 2008), and not necessarily driven by female needs (e.g., Solomon and Jacquot 2002; Wolff 2008). In prairie voles, and many other arvicoline rodents, estrus and ovulation are induced by males (Keller 1985) and not by the presence of other reproductively active females. Thus, induced ovulation may preclude synchronous estrus even if it were adaptive.

Emlen and Oring (1977) argue that synchronous breeding would select for monogamy, which in turn would decrease the intensity of sexual selection in that a few males could not monopolize most of the matings. On the other hand, Wolff and Macdonald (2004) have argued that high levels of promiscuity have the same result. If females mate promiscuously such that all, or most, males obtain some reproductive success, sexual selection is relaxed and runaway selection for any particular trait will not occur. In fact, the promiscuity observed in female prairie voles in several of our studies (e.g., Wolff and Dunlap 2002; Wolff et al. 2002; Ophir et al. 2008), as well as those of others (e.g., Solomon et al. 2004; S. Thomas personal communication (2008)), may be a selecting force for mate-guarding by males and apparent social monogamy observed in this species.

The results of this study showing asynchronous breeding is most consistent with the hypothesis that females seek a mating tactic that optimizes their flexibility in choosing different and (or) multiple mates through time. This tactic might be an adaptation to increase genetic diversity of offspring throughout the breeding life span of a female.

Acknowledgements

This research was supported by National Science Foundation grants to J.O.W. and S.M.P. We thank Shawn Thomas and two anonymous reviewers for helpful comments on an earlier draft of the paper.

Received 28 September 2007. Accepted 10 January 2008. Published on the NRC Research Press Web site at cjz.nrc.ca on 28 March 2008.

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J.O. Wolff. (1) Department of Biological Sciences, St. Cloud State University, St. Cloud, MN 56301, USA.

A.G. Ophir and S.M. Phelps. Department of Zoology, University of Florida, Gainesville, FL 32611, USA.

(1) Corresponding author (e-mail: jowolff@stcloudstate.edu).