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Edited by William T. Although prairie voles Looking Real Sex Fidelity Illinois ochrogaster are socially monogamous, males vary in both sexual and spatial fidelity. Most males form pairbonds, cohabit with one female, and defend territories. Wandering males, in contrast, have expansive home ranges that overlap many males and females. In the laboratory, pairing is regulated by arginine vasopressin and its predominant CNS receptor, vasopressin 1a receptor V1aR.
We investigated individual differences in forebrain V1aR expression of male prairie voles in mixed-sex seminatural enclosures. Individual differences in V1aR were compared with space use measured by radio telemetry and paternity determined with microsatellite markers.
Animals engaging in extra-pair fertilizations EPFs as either wanderers or paired residents overlapped ificantly more in same- and opposite-sex home ranges. Surprisingly, neither social fidelity measured by space use nor sexual fidelity measured by paternity was associated with V1aR expression in the ventral pallidum VPall or lateral septum, areas causally related to pairbond formation.
Individual differences in brain and behavior parallel differences between prairie voles and promiscuous congeners. The concordance among space use, paternity, and V1aR in spatial circuits suggests a common link between the mechanisms of spatial behaviors and success at EPF. The combined data demonstrate how organismal biology can inform our understanding of individual and species differences in behavioral mechanisms. The origin and nature of phenotypic variation has long been a core concern of evolutionary biology 1 — 3. Recent research has demonstrated how variation in small s of genes can cause profound differences within and between species 4 — 6.
Although species differences must have their roots in individual differences, few studies have examined how molecular mechanisms relate to individual variation in natural settings, and fewer still have focused on phenotypes as complex as vertebrate social behavior e. In the current study, we investigate the contributions of a neuroendocrine gene, the vasopressin 1a receptor V1aRto individual differences in male reproductive tactics and mating success among socially monogamous prairie voles Microtus ochrogaster.
Behavioral diversity emerges from an underlying variation in the function of neural circuits; the contribution of V1aR to vole mating systems is a particularly interesting example of such variation. Prairie voles differ from promiscuous congeners in that they form long-term pairbonds, cohabit with a single partner, defend territories, and exhibit paternal care 9. Among males, these species differences in behavior are caused in part by stable differences in V1aR expression within the forebrain 10 Injections of vasopressin AVP antagonists into either the lateral septum LS or the ventral pallidum VPall disrupt pairbonding in male prairie voles but do not alter mating 12 Within prairie voles, individual differences in social behaviors and brain V1aR expression are predicted by variation in a microsatellite adjacent to the prairie vole V1aR promoter Together, these data demonstrate that V1aR function contributes to both intra- and interspecific differences in a complex social behavior.
Such findings serve as a foundation from which to explore the nature and the consequences of variation in brain and behavior in more natural environments. Although prairie voles are considered socially monogamous, in natural settings, a ificant of males and females are single at any given time Based on available field data, males may switch between these tactics In parallel to this behavioral variation, we have documented extraordinary diversity in the regional expression of V1aR Through a combination of functional and neuroanatomical studies, these brain regions have been implicated in spatial memory e.
Does such neural variation relate to patterns of natural behavior? Do measures of mating success provide insights into the persistence of these individual differences? In the current Looking Real Sex Fidelity Illinois, we assess the relationships among male reproductive tactics, neural V1aR expression, and mating success. We used radio telemetry to measure patterns of space use. Together, these data allowed us to ask whether individual differences in V1aR expression in the VPall or LS predicted whether males adopted resident or wandering tactics or were likely to engage in extra-pair fertilizations EPFs.
We next assayed V1aR expression in the PCing and LDThal and asked whether either was related to patterns of male space use or sexual fidelity. By comparing the associations among space use, offspring paternity, and forebrain V1aR, we hope to Looking Real Sex Fidelity Illinois the nature and persistence of neural and behavioral variation in this species. We recovered 43 males and 38 females serving in this experiment 5 males and 10 females died before recovery. Of the surviving animals, two females shed their radio collars and were therefore excluded from analysis involving space use because we were unable to properly assess their home range size or overlap.
A majority of males and females were classified as members of a pair [males, 32 of 43 We assessed the paternity of 99 embryos gathered from 27 pregnant females We were unable to assess the pairing status of one pregnant female who Looking Real Sex Fidelity Illinois her radio collar during radio tracking, and we therefore excluded her from our analyses.
We determined whether the embryos for the remaining 26 females were the result of an in-pair fertilization IPF or an EPF. The methods and for paternity analyses are reported in detail elsewhere Briefly, a ificantly greater proportion of resident males sired offspring than did wandering males Fisher's exact test; successful vs.
Of the 23 successful resident males, 19 sired offspring with their partner alone, and 4 sired offspring outside of the pair.
In our subsequent analyses, we define successful males as those who sired offspring during the course of our experiment. IPF males are defined as resident males who sired offspring only with a partner. For completeness, we also regressed body mass against body length and took the residual mass as a measure of male condition.
Core home range size ranged from 8. Patterns of space use and paternity. To describe how males use space relative to females, we also measured the of females a male could encounter. Similar patterns emerged when we compared space use split by sexual fidelity. In principle, this relationship between extra-pair paternity and space use could be driven by the fact that our definition of EPF males includes both unfaithful residents and successful wanderers, whereas IPF males are always residents.
To examine Looking Real Sex Fidelity Illinois possibility, we calculated the Z scores of male—male overlaps within a reproductive tactic resident or wandererincluding animals that did not mate. We then used these Z scores to ask whether EPF males had more male—male overlaps after correcting for overall differences between resident and wanderer tactics.
We repeated this analysis for male—female overlaps. Because of space constraints, we present only the untransformed data Fig. Because of their important roles in pairbond formation, we expected to find individual differences in V1aR expression between residents and wanderers in the VPall and LS. Similarly, variation in the VPall and LS did not predict whether males exhibited sexual fidelity to a partner.
Variation in V1aR expression reflected in ligand binding. Scale bar: 1 mm. Marginal means are adjusted for variation in average specific binding, a measure of tissue quality see Methods. Raw means and standard errors are provided in Table 1. The ificant multivariate interaction between reproductive tactic and mating success thus reflects V1aR binding across both areas. V1aR expression in spatial circuits predicts space use and paternity.
Marginal means are adjusted for variation in MDThal see Methods. As in the space-use data, we find parallels between successful wanderers and the broader group of EPF males. In both behavioral and neuronal phenotypes, we find that our laboratory-reared animals living in seminatural Looking Real Sex Fidelity Illinois exhibited variation comparable to wild, free-living animals 16 Other researchers report similar patterns of V1aR variation in animals with controlled sexual experience 1524suggesting that the neural differences we report are not caused by the varied experiences of males in these enclosures.
In terms of space use, males adopted the resident and wanderer tactics ly reported On average, successful resident males overlapped few males and just one female Fig. Wanderers overlapped ificantly more males than did residents, and this behavior was associated with a trend toward larger home range sizes. Of the two tactics, resident males are much more likely to fertilize females Because resident males are likely to gain additional fitness advantages through paternal care or infanticide deterrence 25 — 27it seems that residency is the favored tactic, whereas wandering makes the best of a bad situation In our data, tactic was not associated with variation in body size, weight, or condition Table 1 also see ref.
Residents have a longer anogenital distance AGD 29however, which suggests exposure to a more masculinizing Looking Real Sex Fidelity Illinois in utero In prairie voles, long AGD males are preferred by females and have higher sperm counts These traits limit the ability of short AGD males to become successful residents, and thus may favor wandering as an alternative tactic.
Given that a particular male adopted a resident or wandering tactic, the behavioral attributes that predict mating success within those tactics differ substantially Fig. Resident males maximize mating success by processes that facilitate mate guarding, such as reducing the size of the area defended, excluding other males, and centering space use around a single female.
Wandering males, in contrast, were only successful when they overlapped many male and female home ranges, presumably increasing the likelihood of opportunistic mating. Although paired males generally succeeded by mate guarding, a subset was able to obtain EPFs.
Combining space-use data from promiscuous residents and successful wanderers reveals that EPF males as a group are characterized by high same- and opposite-sex overlap Fig. This pattern persists even after correcting for differences in overlap associated with wandering or residency. How is such behavioral variation reflected in neuronal phenotypes? Is there a pattern of forebrain V1aR expression that characterizes individual differences in monogamy? Looking Real Sex Fidelity Illinois first examined the expression of V1aR in the LS and the VPall, two limbic regions in which V1aR function coordinates pairbond formation in the laboratory 13 Based on such causal data, as well as ly documented species differences, we hypothesized that resident and wandering males would differ in the abundance of V1aR expressed in either the LS or the VPall.
Variation in these regions also was Looking Real Sex Fidelity Illinois to predict sexual fidelity Fig. Given that resident males have much greater mating success than wandering males, one interpretation of these findings is that selection favors males who have the ability to form pairbonds 23 and has thus eliminated much of the variation in these structures. Interestingly, Hammock and Young 15 find ificantly correlated variation in laboratory pairbonding, LS V1aR, and the length of a microsatellite at the prairie vole V1aR locus.
Because we did not find a similar relationship between LS and residency, our data indicate that other factors play a greater role in determining individual differences in pairbond formation and sexual fidelity in natural settings.
These factors may include variation in mating frequency and its putative effects on vasopressin release e. We found a ificant interaction between reproductive tactic and mating success that mirrored patterns of space use Figs. Indeed, V1aR in these regions was a good predictor of sexual fidelity in general, particularly in PCing Fig. Interestingly, V1aR expression in PCing also predicts sexual fidelity across vole species. PCing V1aR expression is especially robust in pine voles 24a species thought to be genetically monogamous The strong concordance between space-use measures and V1aR expression in spatial circuits suggests a common Looking Real Sex Fidelity Illinois of these phenotypes to EPF.
PCing and LDThal are strongly connected to one another and to the hippocampus 2236which is central to spatial memory 37 — Neuronal activity and postlesion deficits confirm the role of PCing in spatial learning 18 — 192139whereas some studies associate it with social and emotional memory as well 40 The role of LDThal in spatial memory is less studied 20but our data suggest that its contribution to space-use and extra-pair paternity is weaker than that of PCing.
Last, we note that vasopressin regulates aggression, dominance learning, and social memory in a of rodents 42 — These data lead us to suggest that V1aR expression in PCing and perhaps LDThal modulates memory for the spatial location of aggressive interactions, which influences rates of extra-pair paternity. Wandering, less competitive males should encounter estrus females more often if they intrude into more territories. Similarly, paired males seeking EPFs must leave their own territories to intrude on neighbors.
Among voles and many other taxa, local residents have substantial advantages over intruders 45 — 47and entering the territory of another carries ificant risk of defeat.Looking Real Sex Fidelity Illinois
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