Variation, plasticity, and alternative mating tactics: Revisiting what we know about the socially monogamous prairie vole

Madrid, Jesus E.; Parker, Karen J.; Ophir, Alexander G.

doi:10.1016/bs.asb.2020.02.001

Cited by 40 publications

(51 citation statements)

References 155 publications

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“…Importantly, we note that flexibility in putative mating systems is likely the norm, rather than the exception in animal models. Even the seemingly well-characterized mating system of prairie voles contains surprises revealed only upon extensive observation in naturalistic settings 26 . In some cases, differences in neuropeptide receptor distributions may be detectable in spite of intraspecific (or within-mating system) social variation, but this may less common than previously assumed.…”

Section: Discussionmentioning

confidence: 99%

“…Developments within the field of oxytocin and vasopressin research have also revealed substantial challenges to the interpretation and translation of findings from rodent models to other mammalian groups. Prairie voles exhibit substantial diversity in their mating tactics 26 and their central distribution patterns of nonapeptide receptors [27][28][29] . Reducing any species' socioecology and neurobiology to sets of strictly canalized components might oversimplify the underlying mechanisms and limit insights.…”

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confidence: 99%

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Neural correlates of mating system diversity: oxytocin and vasopressin receptor distributions in monogamous and non-monogamous Eulemur

Grebe

Sharma

Freeman

et al. 2021

Sci Rep

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Contemporary theory that emphasizes the roles of oxytocin and vasopressin in mammalian sociality has been shaped by seminal vole research that revealed interspecific variation in neuroendocrine circuitry by mating system. However, substantial challenges exist in interpreting and translating these rodent findings to other mammalian groups, including humans, making research on nonhuman primates crucial. Both monogamous and non-monogamous species exist within Eulemur, a genus of strepsirrhine primate, offering a rare opportunity to broaden a comparative perspective on oxytocin and vasopressin neurocircuitry with increased evolutionary relevance to humans. We performed oxytocin and arginine vasopressin 1a receptor autoradiography on 12 Eulemur brains from seven closely related species to (1) characterize receptor distributions across the genus, and (2) examine differences between monogamous and non-monogamous species in regions part of putative “pair-bonding circuits”. We find some binding patterns across Eulemur reminiscent of olfactory-guided rodents, but others congruent with more visually oriented anthropoids, consistent with lemurs occupying an ‘intermediary’ evolutionary niche between haplorhine primates and other mammalian groups. We find little evidence of a “pair-bonding circuit” in Eulemur akin to those proposed in previous rodent or primate research. Mapping neuropeptide receptors in these nontraditional species questions existing assumptions and informs proposed evolutionary explanations about the biological bases of monogamy.

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Neural correlates of mating system diversity: oxytocin and vasopressin receptor distributions in monogamous and non-monogamous Eulemur

Grebe

Sharma

Freeman

et al. 2021

Sci Rep

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“…We expect that the availability of these epigenetic clocks will provide a significant boost to the attractiveness of the prairie vole as a biological model in aging research. Prairie voles are perhaps best known for their propensity to form human-like socially monogamous pair bonds 12,13 . The human literature has demonstrated overwhelming evidence that there are a suite of positive health and longevity benefits associated with healthy supportive marriage partnerships.…”

Section: Discussionmentioning

confidence: 99%

“…However, most rodents lack the propensity to form pair bonds, a key feature that is so definitive of humans 10 and relatively rare among mammals in general 11 . Prairie voles (Microtus ochrogaster), on the other hand, are an excellent model species for investigating the neurobiology of complex social behaviors because they form long-term socially monogamous bonds with their mates 12,13 , and both parents exert significant and relatively equal effort to raise their young 14,15 . In laboratory settings, prairie voles that cohabitate and mate with an opposite-sex partner for an extended period (>24 hours) exhibit a robust preference for their partner over a stranger and develop selective aggression toward unfamiliar intruders, whereas sex naïve individuals do not demonstrate these behaviors, which are consistent with a pair bond 16 .…”

Section: Introductionmentioning

confidence: 99%

Pair bonding slows epigenetic aging and alters methylation in brains of prairie voles

Sailer

Haghani

Zoller

et al. 2020

Preprint

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The quality of romantic relationships can be predictive of health consequences related to aging. DNA methylation-based biomarkers of aging have been developed for humans and many other mammals and could be used to assess how pair bonding impacts aging. Prairie voles (Microtus ochrogaster) have emerged as a model to study social attachment among adult pairs. Here we describe DNA methylation-based estimators of age for prairie voles based on novel DNA methylation data generated on highly conserved mammalian CpGs measured with a custom array. The multi-tissue epigenetic clock for voles was trained on 3 tissue sources (ear, liver, and samples of brain tissue from within the pair bonding circuit). A novel dual species human-vole clock accurately measured relative age defined as the ratio of chronological age to maximum age. According to the human-vole clock of relative age, sexually inexperienced voles exhibit accelerated epigenetic aging in brain tissue (p = 0.02) when compared to pair bonded animals of the same chronological age. Epigenome wide association studies identified CpGs in four genes that were strongly associated with pair bonding across the three tissue types (brain, ear, and liver): Hnrnph1, Fancl, Fam13b, and Fzd1. Further, four CpGs (near the Bmp4 exon, Eif4g2 3 prime UTR, Robo1 exon, and Nfat5 intron) exhibited a convergent methylation change between pair bonding and aging. This study describes highly accurate DNA methylation-based estimators of age in prairie voles and provides evidence that pair bonding status modulates the methylome.

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“…Both vole species tested exhibited strong, selective preferences for familiar same-sex peers, despite differences in mating system. Prairie voles typically reside with a mate in socially monogamous partnerships year round, but may also form extended family groups with undispersed offspring, or even multiple breeding females (Getz et al, 1981;Hayes and Solomon, 2004;Madrid et al, 2020). These relationship types are consistent with a high degree of selectivity for familiar individuals, including samesex peers.…”

Section: Species Differencesmentioning

confidence: 99%

Comparative Assessment of Familiarity/Novelty Preferences in Rodents

Beery

Shambaugh

2021

Front. Behav. Neurosci.

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Sociality—i.e., life in social groups—has evolved many times in rodents, and there is considerable variation in the nature of these groups. While many species-typical behaviors have been described in field settings, the use of consistent behavioral assays in the laboratory provides key data for comparisons across species. The preference for interaction with familiar or novel individuals is an important dimension of social behavior. Familiarity preference, in particular, may be associated with more closed, less flexible social groups. The dimension from selectivity to gregariousness has been used as a factor in classification of social group types. Laboratory tests of social choice range from brief (10 minutes) to extended (e.g., 3 hours). As familiarity preferences typically need long testing intervals to manifest, we used 3-hour peer partner preference tests to test for the presence of familiarity preferences in same-sex cage-mates and strangers in rats. We then conducted an aggregated analysis of familiarity preferences across multiple rodent species (adult male and female rats, mice, prairie voles, meadow voles, and female degus) tested with the same protocol. We found a high degree of consistency within species across data sets, supporting the existence of strong, species-typical familiarity preferences in prairie voles and meadow voles, and a lack of familiarity preferences in other species tested. Sociability, or total time spent near conspecifics, was unrelated to selectivity in social preference. These findings provide important background for interpreting the neurobiological mechanisms involved in social behavior in these species.

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Variation, plasticity, and alternative mating tactics: Revisiting what we know about the socially monogamous prairie vole

Cited by 40 publications

References 155 publications

Neural correlates of mating system diversity: oxytocin and vasopressin receptor distributions in monogamous and non-monogamous Eulemur

Neural correlates of mating system diversity: oxytocin and vasopressin receptor distributions in monogamous and non-monogamous Eulemur

Pair bonding slows epigenetic aging and alters methylation in brains of prairie voles

Comparative Assessment of Familiarity/Novelty Preferences in Rodents

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