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. Author manuscript; available in PMC 2015 November 18. Published in final edited form as: . 2014 ; 34(2): 122–128.
Does paedomorphosis contribute to prairie vole monogamy? Timothy Bushyhead and J. Thomas Curtis* Department of Pharmacology and Physiology, Oklahoma State University Center for Health Sciences, Tulsa OK, USA 74107
Abstract Author Manuscript
We examined skull morphology in prairie voles (Microtus ochrogaster) and meadow voles (M. pennsylvanicus), two closely related species with fundamentally different mating systems, to test the hypothesis that paedomorphosis contributes to the evolution of monogamous mating systems. Using several skull measurements, we found that the overall length:width ratio of meadow vole skulls was greater than that of prairie voles suggesting that meadow vole have longer narrower skulls. We then examined which aspects of skull morphology differed between the species and found that the ratio difference was attributable primarily to longer snout length in meadow voles. Finally, we compared adult morphology in both species to that of pups and found the prairie vole, a monogamous species, displays a more juvenile-like skull morphology than does the meadow vole, a promiscuous species. These results suggest that monogamous vole species retain more juvenile-like morphology than do promiscuous species, and thus possibly retain juvenile-like behaviors that may contribute to a monogamous mating system.
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Introduction
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Although monogamy is widely believed be common among birds, monogamous pairings are uncommon among mammals. Practically, this makes sense since care of the young (brooding, feeding, nest defense, etc.) can be shared more-or-less equally by pairs of birds. In contrast, among mammals, some reproductive aspects, for example gestation and feeding, are borne solely by the female. In theory, this should allow male mammals to limit their reproductive contributions to searching out and impregnating as many females as possible, maximizing their chances for genetic representation in the next generation. Why then would any mammalian species develop a monogamous mating strategy? The answer appears to be rooted in differential reproductive success associated with paternal contribution to offspring care (McGuire et al., 1992; Ribble, 1992). In some species, the presence of the male during early development enhances offspring survival. Exactly why this is so is still open to question, but may involve protection from infanticide by other males, continued thermal protection when the female is away from the nest, or other factors that may be species specific. Regardless of the specific mechanism by which male presence increases
*
Correspondence to: J. Thomas Curtis, Ph.D., Department of Pharmacology and Physiology, Oklahoma State University Center for Health Sciences, Tulsa OK 74107, 918 939 8471, [email protected]. T. Bushyhead, M.S., is a third year medical student at the Oklahoma State University Center for Health Sciences.
Author Contributions: Both authors contributed to experimental design. TB performed the photography, detailed skull measurements, and manuscript preparation. JTC performed statistical analyses, graphics production and manuscript preparation.
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reproductive success, it appears that remaining with a single female and the pair’s offspring may maximize his genetic representation in the next generation. However, for males to adopt such a strategy, some male-typical traits may need to be suppressed.
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Male mammals commonly display traits that maximize success in finding and competing for mates. Among these are a tendency to cover a large home range, territoriality and aggression toward conspecifics, and the development of secondary sexual characteristics, the latter of which often produce significant sexual dimorphism between males and females (McPherson and Chenoweth, 2012). However, the same traits that may serve males well when competing for mates may be counter-productive in a monogamous relationship. As such, for monogamy to emerge, counter-productive traits must be suppressed. Importantly, many of these traits emerge as males grow and age, but are lacking in juveniles. Thus, retaining juvenile characteristics such as high levels of sociality, tolerance of conspecifics, huddling behavior, etc., into male adulthood might be an important step in the development of monogamous mating strategies.
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Paedomorphism, and specifically neoteny - the retention of juvenile characteristics - has been invoked as a major factor in human evolution (Bolk, 1926; Gould, 1977), including in the evolution of pair bonding between human adults (Fraley and Shaver, 2000). Relative to our closest primate relatives, humans display a more juvenile morphology, and nowhere is this difference so apparent as in the face. Compared to chimpanzees and gorillas, adult humans display a face and head shape – large cranium, with flat, vertical face – that is similar among juveniles of all three species (although see (Penin et al., 2002) for a dissenting view of the relative role of neoteny in human face shape). As adults, humans lack the prognathic growth pattern displayed by the other species. In other words, humans retain the flat face while our close relatives develop much more prominent jaws and superciliary ridges. It is important to note that behavioral changes and morphological changes may occur in tandem, resulting in juvenile-like behavior as well as juvenile-like form. An excellent example of such parallel development is seen in canids (wolves, foxes, jackals, etc.) selection for “puppy-like” behavior in adult foxes can also produce puppy-like morphology (Trut et al., 2004). In particular, behavioral selection resulted in foxes whose skulls featured notably shorter snouts (Trut et al., 2004). In dogs, there is a correlation between the behavior patterns of dog breeds and the degree of divergence from the “ancestral” body form (Goodwin et al., 1997): behavior patterns typical of infantile wolves are seen in the most physically paedomorphic dog breeds.
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We chose to examine a possible role for paedomorphism in the development of monogamy by comparing skull morphology in two species of vole. Voles are small mammals that are very closely related and quite similar in form, but that display a diverse array of mating strategies (Wolff, 1985). We examined the skulls of prairie voles (Microtus ochrogaster) which have become an important model animal for the study of monogamous pair bonding and biparental care, and meadow voles (M. pennsylvanicus), a species in which males display a promiscuous mating strategy and in which only females care for the young. We show that a monogamous mammal, the prairie vole, displays morphological traits suggesting that the retention of juvenile characteristics by adult males may have contributed to the development of a monogamous mating strategy. The results provide support for the idea that
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paedomorphosis may have played a role in the evolution of human social structures (Fraley and Shaver, 2000).
Methods Specimens and preparation
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All vole skull specimens were acquired from captive breeding colonies at either Florida State University, USA or at the Oklahoma State University Center for Health Sciences, USA. Care and housing of the animals, and the methods for euthanasia (anesthetic overdose or CO2 asphyxiation) were approved by the Institutional Animal Care and Use Committees at the respective universities. Prairie and meadow voles that were retired breeders, unmanipulated control animals from which brain tissue was not needed, or that otherwise were unsuited for other experiments due to mismatches in age or size, were humanely euthanized, and the heads were removed, frozen (−20C°), and retained for further study. Freezer storage duration varied from 1 week to approximately 8 years. During the final preparation steps, specimens were allowed to thaw for 12-24 hours, most of the fur was removed, and dermestid beetle larvae (Dermestes maculatus) were used to remove the remaining soft tissue. After processing by the beetle larvae, the specimens were dipped in a 70% ethanol solution for ~30 sec. and then re-frozen for ~24 hrs to ensure that any remaining larvae were destroyed. Skulls and disarticulated mandibles then were stored at room temperature. Totals of 129 prairie vole and 30 meadow vole skulls were used in the analyses. Morphometrics
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Skulls were consistently positioned, and digitally photographed and measured using an AMG dissecting microscope/digital camera and Micron software (both from Westover Scientific, Mill Creek WA, USA). The system was calibrated at 0.65x magnification and all images were captured at that magnification with only minimal fine focus adjustment to accommodate various skull sizes. Contrast and brightness settings were adjusted for most images. Most skulls were photographed in three positions: dorsal view, ventral view, and lateral view. Landmarks for measurement were chosen based on relevant literature, and ease and consistency of measurement. Some skulls did not provide sufficient landmark integrity to perform satisfactory measurements for all variables (e.g., on some skulls, the zygomatic arch was damaged on one side, so width measurements were not made from those individuals).
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All measurements were made from photographs. Four aspects of skull morphology (Fig 1.) were measured to the nearest 0.01 mm using the Micron software: the overall length of the skull and the zygomatic width were used to define the length:width ratio of the skull, while the remaining two measures (cranial and snout lengths) were used test the prediction that differences in skull morphology would be driven primarily by snout length, as would be expected if paedomorphosis contributed to the development of vole monogamy. Measurements and ratios are presented as means ± sem.
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One-, two-, and three-way ANOVA’s with Student-Newman-Keuls pairwise comparisons to probe significant main effects and interactions, and t-tests were used for statistical analyses. We compared skull measurements between species using known-age groupings. We choose the cut-off ages for the groups based on vole biology and on age categories typically applied to voles used in laboratory experiments. In these species, reports suggest that the earliest onset of sexual activity occurs at about thirty days of age (Nadeau, 1985). Thus, group 1 included voles that were 30 days of age or younger. Group 2 included voles that were between 30 and 60 days of age. A cut-off of sixty for this group was chosen based on the typical age at which voles are considered old enough for use in behavioral and other experiments examining adult social behavior (e.g., (McGuire and Novak, 1987). Voles between 60 and 130 days of age comprised group 3 as this age range is typical for voles used in laboratory research. Finally, group 4 included all animals greater than 130 days of age.
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Results
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The were no species or sex differences in ages at termination (species, F1,119 = 1.00, p = 0.32; sex, F1,119 = 0.57, p = 0.45). An overall ANOVA revealed that there was no main effect of sex for any measure, thus the sexes were combined in subsequent morphological comparisons. There were main effects of age for cranial length and skull width, and main effects of both age and species for overall skull length, snout length, and the overall length to width (L:W) ratio (Table 1). There was a main effect of species only for the cranial length:snout length ratio. Obviously, the four primary measurements for pups (4 - 21 days of age, n = 35) were significantly different from those of older animals. Importantly though, there were no significant differences between pups of the two species for any measure, showing that the two species do not differ in skull morphology during the early stages of development. When compared to the L:W ratio for the typical pup (all pups combined), the ratio for adult meadow voles diverged significantly more from the pup-like morphology than did the ratio for prairie voles (meadow voles 0.19 ± 0.01, prairie voles 0.12 ± 0.01; t = 4.93, p < 0.0001) (Fig. 2).
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There are several ways that species differences in skull morphology can arise. Among mammals, a prominent difference between adults and juveniles is seen for snout length. This pattern appears to hold for voles - Carleton (Carlton, 1985) describes the growth of Microtine skulls as follows: “…as the skull enlarges, the proportional relationship of the facial and cranial regions shifts from relatively short rostrum and wide brain case to an elongate, narrower configuration…”. In other words, the development of vole skulls follows the typical mammalian pattern of shifting from a short round head to a longer head with a more pronounced snout (Fig. 1B). If paedomorphosis contributed to the development of the species typical social structures in the voles, we expected that it would be reflected in snout length. This appears to be the case. Among adults, there were no significant differences in skull width (F1,119 = 1.00, p > 0.31) or in cranium length (F1,119 = 3.52, p > 0.06), but there was a significant difference in the overall lengths of the skulls from the two species (F1,119 = 10.06, p < 0.002) and the overall L:W ratio differed between prairie and meadow voles (Fig. 2; F1,119 = 26.50, p < 0.001). Since the skull width and cranial length did not differ, the differences in overall skull length and in the L:W ratio were driven largely by species . Author manuscript; available in PMC 2015 November 18.
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differences in snout length - meadow voles had significantly longer snouts (7.57 ± 0.05mm) than did prairie voles (6.72 ± 0.08mm; F1,119 = 19.78, p < 0.001).
Discussion
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We compared the skull morphologies of two vole species with differing mating systems to test the hypothesis that paedomorphosis may contribute to the development of a monogamous mating system. The prairie voles used in this study derive from a southern Illinois (USA) population. Voles from this population are considered to have a monogamous mating system (Getz and Carter, 1980) and have been used for social bonding studies for several decades. Prairie vole males display high levels of selective affiliation toward related kin, extensive parental care, and nest sharing; all of which are traits shared with juveniles. In contrast, meadow voles typically are considered to display a promiscuous mating system (Dewsbury, 1981). This latter species displays generalized aggression, strong intolerance of conspecifics except for brief contact associated with mating, and males provide no parental care. This is in contrast to the behaviors of juvenile meadow vole which are behaviorally quite similar to prairie vole pups. Thus, adult male prairie voles display more juvenile-like behaviors than do meadow voles. We predicted that the skull of the prairie vole, a monogamous vole species, would display a more juvenile-like morphology than would that of the meadow vole, a promiscuous species. This prediction was borne out. Prairie voles had shorter overall skull lengths, primarily due to having shorter snouts. As a result adult prairie voles’ skulls were more like those of pups than were adult meadow vole skulls, which is consistent with our overall hypothesis.
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The differences that we found in skull morphology in monogamous vs. promiscuous voles are consistent with reports of physiological and behavioral differences that suggest that the development of pups of monogamous species is delayed relative to that of pups from promiscuous species. In general, pups of promiscuous meadow and montane voles show more rapid behavioral and physiological development than do pups of monogamous pine and prairie voles (McGuire and Novak, 1984, 1986; Nadeau, 1985; Prohazka et al., 1986). Relative to monogamous species, promiscuous voles display more advanced neuromuscular development at five days of age, and become independent earlier, eating solid food as early as 8 days of age and weaning at 13-14 days. Monogamous vole pups are not weaned until about one week later. In addition, monogamous species take longer to reach sexual maturity.
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The timing of postnatal brain development also differs between monogamous and promiscuous species (Gutierrez et al., 1989). The temporal patterns of thymidine kinase (TK, an index of cell proliferation) activity in the cerebrum suggest that pine voles (a monogamous species) are still undergoing considerable mitotic activity at five days postnatally. In contrast, meadow voles at the same age show evidence of significantly reduced mitotic activity - more like that seen in other non-pair-bonding species such as rats and mice (Gutierrez et al., 1989). A similar species-specific pattern of TK activity is seen in the cerebellum where pine voles show evidence of a significant increase in cell proliferation between 2 and 5 days of age (Gutierrez et al., 1989). This increase is much less in meadow voles, again suggesting that brain development is delayed in monogamous voles and may account for the more advanced neuromuscular development displayed by promiscuous vole
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pups mentioned above (Prohazka et al., 1986). Moreover, promiscuous voles achieve adult patterns of some brain chemicals earlier than do monogamous voles. Brain derived neurotrophic factor (BDNF) is important in the proliferation, survival and growth of neurons. In some brain areas the promiscuous meadow vole displayed adult patterns of BDNF expression at about two weeks of age, while the monogamous prairie vole did not show adult patterns until at least three weeks of age (Liu et al., 2001). It is interesting to note that the timing of the switch to adult patterns of BDNF expression to some extent parallels the timing of weaning and independence in each species.
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These results have important implications regarding the evolution of strong attachments between adult humans in general, and for adult pair-bonding in particular. Humans typically are considered to be monogamous. Worldwide, the vast majority of individuals of both sexes “marry”, and, even in cultures where multiple partners are permitted, monogamous pairing is the modal arrangement (Fisher, 1989). In a phylogenetic analysis of adult attachment behaviors, Fraley et al. (Fraley and Shaver, 2000) noted that mammalian species that display adult attachments are more likely than others to be characterized by “… developmental immaturity or neoteny …”. Our finding that adult prairie voles have a skull morphology that is more similar to that of vole pups than is that for meadow voles is consistent with the hypothesis that paedomorphosis contributed the development of a monogamous mating system in prairie voles, and thus potentially in other mammals. Finally, and in line with our hypothesis that paedomorphosis was important in the development of adult pair-bonding in general, especially in males, morphological effects that accompanied selection for juvenile behavior in foxes were much more apparent in males than in females (Trut et al., 2004). Notable in those studies was the observation that the selection for juvenile behaviors in foxes that produced juvenile morphology also altered functioning of the mesocorticolimbic dopamine system(Trut et al., 2000), which plays an important role in the formation and/or expression of adult pair bonds both in voles (Curtis et al., 2006) and in humans (Fisher et al., 2005).
Acknowledgements This research was supported in part by NIH grant HD48462.
References
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Bolk L. On the problem of Anthropogenesis. Ams Proc. 1926; 29:465–475. Carlton MD. Tamarin RH. Macroanatomy. Biology of New World Microtus American Society of Mammalogists. 1985:254–285. Special Publication No 8. Curtis JT, Liu Y, Aragona BJ, Wang ZX. Dopamine and monogamy. Brain Res. 2006; 1126:76–90. [PubMed: 16950234] Dewsbury DA. An exercise in the prediction of monogamy in the field from laboratory data on 42 species of Muroid rodents. Biologist. 1981; 63:138–162. Fisher H, Aron A, Brown LL. Romantic love: an fMRI study of a neural mechanism for mate choice. J Comp Neurol. 2005; 493:58–62. [PubMed: 16255001] Fisher HE. Evolution of human serial pairbonding. Am. J. Phys. Anthrop. 1989; 78:331–354. [PubMed: 2929738] Fraley RC, Shaver PR. Adult attachment theory: theoretical developments, emerging controversies, and unanswered questions. Rev Gen Psychol. 2000; 4:132–154.
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Getz LL, Carter CS. Social organization in Microtus ochrogaster populations. Biologist. 1980; 62:56– 69. Goodwin D, Bradshaw JWS, Wickens SM. Paedomorphosis affects agonistic visual signal of domestic dogs. Anim Behav. 1997; 53:297–304. Gould, SJ. Ontogeny and Phylogeny. Harvard University Press; Cambridge MA: 1977. Gutierrez PJ, Meyer JS, Novak M. Comparison of postnatal brain development in meadow voles (Microtus pennsylvanicus) and pine voles (M. pinatorum). J Mammal. 1989; 70:292–299. Liu Y, Fowler CD, Wang Z. Ontogeny of brain-derived neurotrophic factor gene expression in the forebrain of prairie and montane voles. Brain Res Dev Brain Res. 2001; 127:51–61. [PubMed: 11287064] McGuire B, Novak M. A comparison of maternal behaviour in the meadow vole (Microtus pennsylvanicus), prairie vole (M. ochrogaster) and pine vole (M. pinatorum). Anim Behav. 1984; 32:1132–1141. McGuire B, Novak M. Parental care and its relationship to social organization in the montane vole (Microtus montanus). J. Mammal. 1986; 67:305–311. McGuire B, Novak M. The effects of cross-fostering on the development of social preferences in meadow voles (Microtus pennsylvanicus). Behav Neural Biol. 1987; 47:167–172. [PubMed: 3555453] McGuire B, Russell KD, Mahoney T, Novak M. The effects of mate removal on pregnancy success in prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus). Biol Reprod. 1992; 47:37–42. [PubMed: 1637945] McPherson FJ, Chenoweth PJ. Mammalian sexual dimorphism. Anim Reprod Sci. 2012; 131:109–122. [PubMed: 22482798] Nadeau JH. Tamarin RH. Ontogeny. Biology of New World Microtus. American Society of Mammalogists. 1985:254–285. Special Publication No. 8. Penin X, Berge C, Baylac M. Ontogenetic study of the skull in modern humans and the common chimpanzees: neotenic hypothesis reconsidered with a tridimensional procrustes analysis. Am. J. Phys. Anthrop. 2002; 118:50–62. [PubMed: 11953945] Prohazka D, Novak MA, Meyer JS. Divergent effects of early hydrocortisone treatment on behavioral and brain development in meadow and pine voles. Dev Psychobiol. 1986; 19:521–535. [PubMed: 3542640] Ribble DO. Lifetime reproductive success and its correlates in the monogamous rodent, Peromyscus californicus. J Anim Ecol. 1992; 61:457–468. Trut LN, Plyusnina IZ, Kolesnikova LA, Kozlova ON. Interhemispheral neurochemical differences in brains of silver foxes selected for behavior and the problem of directional asymmetry. Russ J Genet. 2000; 36:776–780. Trut LN, Plyusnina IZ, Oskina IN. An experiment on fox domestication and debatable issues of evolution of the dog. Russ J Genet s. 2004; 40:644–655. Wolff JO. Tamarin RH. Behavior. Biology of New World Microtus, American Society of Mammalogists. 1985:340–372. Special Publication No 8.
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Figure 1.
Vole skull measurements. Panel a - the distance between the most rostral aspect of the foramen magnum and the most rostral aspect of the incisors was used as an index of overall skull length (A). Zygomatic breadth (B) was used as an index of skull width. Cranial length (C) was defined as the distance along the midline between lambda and the nasofrontal suture. Snout length (D) was defined as the rostrocaudal length of the nasal bone. Panel b – age progression of skull sizes for prairie voles. Scale bars = 10 mm.
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Figure 2.
Relative positions of adult and juvenile prairie and meadow voles on a skull length:skull width continuum. Pups of the two species did not differ (either on this continuum or for any of the other measures). Adult meadow voles diverged significantly more from the juvenile morphology than did prairie voles, suggesting that adult prairie voles retain a more juvenilelike morphology.
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Table 1
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Comparisons of skull measurements between prairie voles (PV) and meadow voles (MV) by age class. Gross measurements (mm) Age (days)
ασ
α
Ratios
α
Sp.
Overall length (A)
Cranial length (B)
Snout σ length (C)
Width (D)
MV
18.50 ± 1.22
13.42 ± 0.59
4.46 ± 0.40
11.70 ± 0.52
1.58 ± 0.07
3.03 ± 0.16
α
ασ
A/D
σ
B/C
0-30 PV
17.55 ± 0.08
12.56 ± 0.37
4.15 ± 0.24
11.14 ± 0.41
1.56 ± 0.02
3.20 ± 0.10
MV
25.18 ± 0.37
15.45 ± 0.26
7.02 ± .025
14.48 ± 0.23
1.74 ± 0.01
2.21 ± 0.06
31-65 PV
25.53 ± 0.84
15.35 ± 0.58
5.98 ± 0.28
14.30 ± 0.39
1.64 ± 0.02
2.60 ± 0.18
MV
26.84 ± .098
15.97 ± 0.40
7.56 ±0.40
15.39 ± 0.43
1.74 ± 0.03
2.12 ±0.12
66-130 PV
25.04 ± 0.17
15.32 ± 0.13
6.57 ± 0.12
14.77 ± 0.11
1.70 ± 0.01
2.35 ±0.04
MV
28.08 ± 0.36
16.50 ± 0.21
7.81 ± 0.14
15.71 ± 0.15
1.79 ± 0.01
2.12 ± 0.03
PV
26.26 ± 0.19
15.98 ± 0.10
6.98 ± 0.08
15.37 ± 0.09
1.71 ± 0.01
2.30 ± 0.02
131+
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Species Means
MV
15.80 ± 0.25
14.51 ± 0.35
PV
14.99 ±0.17
14.10 ± 0.20
SNK pair-wise comparisons were performed only on overall means, significantly different values are joined by brackets (}).
α
- significant main effect of age,
σ
- significant main effect of species.
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. Author manuscript; available in PMC 2015 November 18. Published in final edited form as: . 2014 ; 34(2): 122–128.
Does paedomorphosis contribute to prairie vole monogamy? Timothy Bushyhead and J. Thomas Curtis* Department of Pharmacology and Physiology, Oklahoma State University Center for Health Sciences, Tulsa OK, USA 74107
Abstract Author Manuscript
We examined skull morphology in prairie voles (Microtus ochrogaster) and meadow voles (M. pennsylvanicus), two closely related species with fundamentally different mating systems, to test the hypothesis that paedomorphosis contributes to the evolution of monogamous mating systems. Using several skull measurements, we found that the overall length:width ratio of meadow vole skulls was greater than that of prairie voles suggesting that meadow vole have longer narrower skulls. We then examined which aspects of skull morphology differed between the species and found that the ratio difference was attributable primarily to longer snout length in meadow voles. Finally, we compared adult morphology in both species to that of pups and found the prairie vole, a monogamous species, displays a more juvenile-like skull morphology than does the meadow vole, a promiscuous species. These results suggest that monogamous vole species retain more juvenile-like morphology than do promiscuous species, and thus possibly retain juvenile-like behaviors that may contribute to a monogamous mating system.
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Introduction
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Although monogamy is widely believed be common among birds, monogamous pairings are uncommon among mammals. Practically, this makes sense since care of the young (brooding, feeding, nest defense, etc.) can be shared more-or-less equally by pairs of birds. In contrast, among mammals, some reproductive aspects, for example gestation and feeding, are borne solely by the female. In theory, this should allow male mammals to limit their reproductive contributions to searching out and impregnating as many females as possible, maximizing their chances for genetic representation in the next generation. Why then would any mammalian species develop a monogamous mating strategy? The answer appears to be rooted in differential reproductive success associated with paternal contribution to offspring care (McGuire et al., 1992; Ribble, 1992). In some species, the presence of the male during early development enhances offspring survival. Exactly why this is so is still open to question, but may involve protection from infanticide by other males, continued thermal protection when the female is away from the nest, or other factors that may be species specific. Regardless of the specific mechanism by which male presence increases
*
Correspondence to: J. Thomas Curtis, Ph.D., Department of Pharmacology and Physiology, Oklahoma State University Center for Health Sciences, Tulsa OK 74107, 918 939 8471, [email protected]. T. Bushyhead, M.S., is a third year medical student at the Oklahoma State University Center for Health Sciences.
Author Contributions: Both authors contributed to experimental design. TB performed the photography, detailed skull measurements, and manuscript preparation. JTC performed statistical analyses, graphics production and manuscript preparation.
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reproductive success, it appears that remaining with a single female and the pair’s offspring may maximize his genetic representation in the next generation. However, for males to adopt such a strategy, some male-typical traits may need to be suppressed.
Author Manuscript
Male mammals commonly display traits that maximize success in finding and competing for mates. Among these are a tendency to cover a large home range, territoriality and aggression toward conspecifics, and the development of secondary sexual characteristics, the latter of which often produce significant sexual dimorphism between males and females (McPherson and Chenoweth, 2012). However, the same traits that may serve males well when competing for mates may be counter-productive in a monogamous relationship. As such, for monogamy to emerge, counter-productive traits must be suppressed. Importantly, many of these traits emerge as males grow and age, but are lacking in juveniles. Thus, retaining juvenile characteristics such as high levels of sociality, tolerance of conspecifics, huddling behavior, etc., into male adulthood might be an important step in the development of monogamous mating strategies.
Author Manuscript
Paedomorphism, and specifically neoteny - the retention of juvenile characteristics - has been invoked as a major factor in human evolution (Bolk, 1926; Gould, 1977), including in the evolution of pair bonding between human adults (Fraley and Shaver, 2000). Relative to our closest primate relatives, humans display a more juvenile morphology, and nowhere is this difference so apparent as in the face. Compared to chimpanzees and gorillas, adult humans display a face and head shape – large cranium, with flat, vertical face – that is similar among juveniles of all three species (although see (Penin et al., 2002) for a dissenting view of the relative role of neoteny in human face shape). As adults, humans lack the prognathic growth pattern displayed by the other species. In other words, humans retain the flat face while our close relatives develop much more prominent jaws and superciliary ridges. It is important to note that behavioral changes and morphological changes may occur in tandem, resulting in juvenile-like behavior as well as juvenile-like form. An excellent example of such parallel development is seen in canids (wolves, foxes, jackals, etc.) selection for “puppy-like” behavior in adult foxes can also produce puppy-like morphology (Trut et al., 2004). In particular, behavioral selection resulted in foxes whose skulls featured notably shorter snouts (Trut et al., 2004). In dogs, there is a correlation between the behavior patterns of dog breeds and the degree of divergence from the “ancestral” body form (Goodwin et al., 1997): behavior patterns typical of infantile wolves are seen in the most physically paedomorphic dog breeds.
Author Manuscript
We chose to examine a possible role for paedomorphism in the development of monogamy by comparing skull morphology in two species of vole. Voles are small mammals that are very closely related and quite similar in form, but that display a diverse array of mating strategies (Wolff, 1985). We examined the skulls of prairie voles (Microtus ochrogaster) which have become an important model animal for the study of monogamous pair bonding and biparental care, and meadow voles (M. pennsylvanicus), a species in which males display a promiscuous mating strategy and in which only females care for the young. We show that a monogamous mammal, the prairie vole, displays morphological traits suggesting that the retention of juvenile characteristics by adult males may have contributed to the development of a monogamous mating strategy. The results provide support for the idea that
. Author manuscript; available in PMC 2015 November 18.
Bushyhead and Curtis
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paedomorphosis may have played a role in the evolution of human social structures (Fraley and Shaver, 2000).
Methods Specimens and preparation
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All vole skull specimens were acquired from captive breeding colonies at either Florida State University, USA or at the Oklahoma State University Center for Health Sciences, USA. Care and housing of the animals, and the methods for euthanasia (anesthetic overdose or CO2 asphyxiation) were approved by the Institutional Animal Care and Use Committees at the respective universities. Prairie and meadow voles that were retired breeders, unmanipulated control animals from which brain tissue was not needed, or that otherwise were unsuited for other experiments due to mismatches in age or size, were humanely euthanized, and the heads were removed, frozen (−20C°), and retained for further study. Freezer storage duration varied from 1 week to approximately 8 years. During the final preparation steps, specimens were allowed to thaw for 12-24 hours, most of the fur was removed, and dermestid beetle larvae (Dermestes maculatus) were used to remove the remaining soft tissue. After processing by the beetle larvae, the specimens were dipped in a 70% ethanol solution for ~30 sec. and then re-frozen for ~24 hrs to ensure that any remaining larvae were destroyed. Skulls and disarticulated mandibles then were stored at room temperature. Totals of 129 prairie vole and 30 meadow vole skulls were used in the analyses. Morphometrics
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Skulls were consistently positioned, and digitally photographed and measured using an AMG dissecting microscope/digital camera and Micron software (both from Westover Scientific, Mill Creek WA, USA). The system was calibrated at 0.65x magnification and all images were captured at that magnification with only minimal fine focus adjustment to accommodate various skull sizes. Contrast and brightness settings were adjusted for most images. Most skulls were photographed in three positions: dorsal view, ventral view, and lateral view. Landmarks for measurement were chosen based on relevant literature, and ease and consistency of measurement. Some skulls did not provide sufficient landmark integrity to perform satisfactory measurements for all variables (e.g., on some skulls, the zygomatic arch was damaged on one side, so width measurements were not made from those individuals).
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All measurements were made from photographs. Four aspects of skull morphology (Fig 1.) were measured to the nearest 0.01 mm using the Micron software: the overall length of the skull and the zygomatic width were used to define the length:width ratio of the skull, while the remaining two measures (cranial and snout lengths) were used test the prediction that differences in skull morphology would be driven primarily by snout length, as would be expected if paedomorphosis contributed to the development of vole monogamy. Measurements and ratios are presented as means ± sem.
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One-, two-, and three-way ANOVA’s with Student-Newman-Keuls pairwise comparisons to probe significant main effects and interactions, and t-tests were used for statistical analyses. We compared skull measurements between species using known-age groupings. We choose the cut-off ages for the groups based on vole biology and on age categories typically applied to voles used in laboratory experiments. In these species, reports suggest that the earliest onset of sexual activity occurs at about thirty days of age (Nadeau, 1985). Thus, group 1 included voles that were 30 days of age or younger. Group 2 included voles that were between 30 and 60 days of age. A cut-off of sixty for this group was chosen based on the typical age at which voles are considered old enough for use in behavioral and other experiments examining adult social behavior (e.g., (McGuire and Novak, 1987). Voles between 60 and 130 days of age comprised group 3 as this age range is typical for voles used in laboratory research. Finally, group 4 included all animals greater than 130 days of age.
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Results
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The were no species or sex differences in ages at termination (species, F1,119 = 1.00, p = 0.32; sex, F1,119 = 0.57, p = 0.45). An overall ANOVA revealed that there was no main effect of sex for any measure, thus the sexes were combined in subsequent morphological comparisons. There were main effects of age for cranial length and skull width, and main effects of both age and species for overall skull length, snout length, and the overall length to width (L:W) ratio (Table 1). There was a main effect of species only for the cranial length:snout length ratio. Obviously, the four primary measurements for pups (4 - 21 days of age, n = 35) were significantly different from those of older animals. Importantly though, there were no significant differences between pups of the two species for any measure, showing that the two species do not differ in skull morphology during the early stages of development. When compared to the L:W ratio for the typical pup (all pups combined), the ratio for adult meadow voles diverged significantly more from the pup-like morphology than did the ratio for prairie voles (meadow voles 0.19 ± 0.01, prairie voles 0.12 ± 0.01; t = 4.93, p < 0.0001) (Fig. 2).
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There are several ways that species differences in skull morphology can arise. Among mammals, a prominent difference between adults and juveniles is seen for snout length. This pattern appears to hold for voles - Carleton (Carlton, 1985) describes the growth of Microtine skulls as follows: “…as the skull enlarges, the proportional relationship of the facial and cranial regions shifts from relatively short rostrum and wide brain case to an elongate, narrower configuration…”. In other words, the development of vole skulls follows the typical mammalian pattern of shifting from a short round head to a longer head with a more pronounced snout (Fig. 1B). If paedomorphosis contributed to the development of the species typical social structures in the voles, we expected that it would be reflected in snout length. This appears to be the case. Among adults, there were no significant differences in skull width (F1,119 = 1.00, p > 0.31) or in cranium length (F1,119 = 3.52, p > 0.06), but there was a significant difference in the overall lengths of the skulls from the two species (F1,119 = 10.06, p < 0.002) and the overall L:W ratio differed between prairie and meadow voles (Fig. 2; F1,119 = 26.50, p < 0.001). Since the skull width and cranial length did not differ, the differences in overall skull length and in the L:W ratio were driven largely by species . Author manuscript; available in PMC 2015 November 18.
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differences in snout length - meadow voles had significantly longer snouts (7.57 ± 0.05mm) than did prairie voles (6.72 ± 0.08mm; F1,119 = 19.78, p < 0.001).
Discussion
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We compared the skull morphologies of two vole species with differing mating systems to test the hypothesis that paedomorphosis may contribute to the development of a monogamous mating system. The prairie voles used in this study derive from a southern Illinois (USA) population. Voles from this population are considered to have a monogamous mating system (Getz and Carter, 1980) and have been used for social bonding studies for several decades. Prairie vole males display high levels of selective affiliation toward related kin, extensive parental care, and nest sharing; all of which are traits shared with juveniles. In contrast, meadow voles typically are considered to display a promiscuous mating system (Dewsbury, 1981). This latter species displays generalized aggression, strong intolerance of conspecifics except for brief contact associated with mating, and males provide no parental care. This is in contrast to the behaviors of juvenile meadow vole which are behaviorally quite similar to prairie vole pups. Thus, adult male prairie voles display more juvenile-like behaviors than do meadow voles. We predicted that the skull of the prairie vole, a monogamous vole species, would display a more juvenile-like morphology than would that of the meadow vole, a promiscuous species. This prediction was borne out. Prairie voles had shorter overall skull lengths, primarily due to having shorter snouts. As a result adult prairie voles’ skulls were more like those of pups than were adult meadow vole skulls, which is consistent with our overall hypothesis.
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The differences that we found in skull morphology in monogamous vs. promiscuous voles are consistent with reports of physiological and behavioral differences that suggest that the development of pups of monogamous species is delayed relative to that of pups from promiscuous species. In general, pups of promiscuous meadow and montane voles show more rapid behavioral and physiological development than do pups of monogamous pine and prairie voles (McGuire and Novak, 1984, 1986; Nadeau, 1985; Prohazka et al., 1986). Relative to monogamous species, promiscuous voles display more advanced neuromuscular development at five days of age, and become independent earlier, eating solid food as early as 8 days of age and weaning at 13-14 days. Monogamous vole pups are not weaned until about one week later. In addition, monogamous species take longer to reach sexual maturity.
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The timing of postnatal brain development also differs between monogamous and promiscuous species (Gutierrez et al., 1989). The temporal patterns of thymidine kinase (TK, an index of cell proliferation) activity in the cerebrum suggest that pine voles (a monogamous species) are still undergoing considerable mitotic activity at five days postnatally. In contrast, meadow voles at the same age show evidence of significantly reduced mitotic activity - more like that seen in other non-pair-bonding species such as rats and mice (Gutierrez et al., 1989). A similar species-specific pattern of TK activity is seen in the cerebellum where pine voles show evidence of a significant increase in cell proliferation between 2 and 5 days of age (Gutierrez et al., 1989). This increase is much less in meadow voles, again suggesting that brain development is delayed in monogamous voles and may account for the more advanced neuromuscular development displayed by promiscuous vole
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pups mentioned above (Prohazka et al., 1986). Moreover, promiscuous voles achieve adult patterns of some brain chemicals earlier than do monogamous voles. Brain derived neurotrophic factor (BDNF) is important in the proliferation, survival and growth of neurons. In some brain areas the promiscuous meadow vole displayed adult patterns of BDNF expression at about two weeks of age, while the monogamous prairie vole did not show adult patterns until at least three weeks of age (Liu et al., 2001). It is interesting to note that the timing of the switch to adult patterns of BDNF expression to some extent parallels the timing of weaning and independence in each species.
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These results have important implications regarding the evolution of strong attachments between adult humans in general, and for adult pair-bonding in particular. Humans typically are considered to be monogamous. Worldwide, the vast majority of individuals of both sexes “marry”, and, even in cultures where multiple partners are permitted, monogamous pairing is the modal arrangement (Fisher, 1989). In a phylogenetic analysis of adult attachment behaviors, Fraley et al. (Fraley and Shaver, 2000) noted that mammalian species that display adult attachments are more likely than others to be characterized by “… developmental immaturity or neoteny …”. Our finding that adult prairie voles have a skull morphology that is more similar to that of vole pups than is that for meadow voles is consistent with the hypothesis that paedomorphosis contributed the development of a monogamous mating system in prairie voles, and thus potentially in other mammals. Finally, and in line with our hypothesis that paedomorphosis was important in the development of adult pair-bonding in general, especially in males, morphological effects that accompanied selection for juvenile behavior in foxes were much more apparent in males than in females (Trut et al., 2004). Notable in those studies was the observation that the selection for juvenile behaviors in foxes that produced juvenile morphology also altered functioning of the mesocorticolimbic dopamine system(Trut et al., 2000), which plays an important role in the formation and/or expression of adult pair bonds both in voles (Curtis et al., 2006) and in humans (Fisher et al., 2005).
Acknowledgements This research was supported in part by NIH grant HD48462.
References
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Figure 1.
Vole skull measurements. Panel a - the distance between the most rostral aspect of the foramen magnum and the most rostral aspect of the incisors was used as an index of overall skull length (A). Zygomatic breadth (B) was used as an index of skull width. Cranial length (C) was defined as the distance along the midline between lambda and the nasofrontal suture. Snout length (D) was defined as the rostrocaudal length of the nasal bone. Panel b – age progression of skull sizes for prairie voles. Scale bars = 10 mm.
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Figure 2.
Relative positions of adult and juvenile prairie and meadow voles on a skull length:skull width continuum. Pups of the two species did not differ (either on this continuum or for any of the other measures). Adult meadow voles diverged significantly more from the juvenile morphology than did prairie voles, suggesting that adult prairie voles retain a more juvenilelike morphology.
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Table 1
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Comparisons of skull measurements between prairie voles (PV) and meadow voles (MV) by age class. Gross measurements (mm) Age (days)
ασ
α
Ratios
α
Sp.
Overall length (A)
Cranial length (B)
Snout σ length (C)
Width (D)
MV
18.50 ± 1.22
13.42 ± 0.59
4.46 ± 0.40
11.70 ± 0.52
1.58 ± 0.07
3.03 ± 0.16
α
ασ
A/D
σ
B/C
0-30 PV
17.55 ± 0.08
12.56 ± 0.37
4.15 ± 0.24
11.14 ± 0.41
1.56 ± 0.02
3.20 ± 0.10
MV
25.18 ± 0.37
15.45 ± 0.26
7.02 ± .025
14.48 ± 0.23
1.74 ± 0.01
2.21 ± 0.06
31-65 PV
25.53 ± 0.84
15.35 ± 0.58
5.98 ± 0.28
14.30 ± 0.39
1.64 ± 0.02
2.60 ± 0.18
MV
26.84 ± .098
15.97 ± 0.40
7.56 ±0.40
15.39 ± 0.43
1.74 ± 0.03
2.12 ±0.12
66-130 PV
25.04 ± 0.17
15.32 ± 0.13
6.57 ± 0.12
14.77 ± 0.11
1.70 ± 0.01
2.35 ±0.04
MV
28.08 ± 0.36
16.50 ± 0.21
7.81 ± 0.14
15.71 ± 0.15
1.79 ± 0.01
2.12 ± 0.03
PV
26.26 ± 0.19
15.98 ± 0.10
6.98 ± 0.08
15.37 ± 0.09
1.71 ± 0.01
2.30 ± 0.02
131+
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Species Means
MV
15.80 ± 0.25
14.51 ± 0.35
PV
14.99 ±0.17
14.10 ± 0.20
SNK pair-wise comparisons were performed only on overall means, significantly different values are joined by brackets (}).
α
- significant main effect of age,
σ
- significant main effect of species.
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