Estrous phase alters social behavior in a polygynous but not a monogamous Peromyscus species

The social organization of rodent species determines behavioral patterns for both affiliative and agonistic encounters. The neuropeptide oxytocin has been implicated in the mediation of social behavior; however, variability in both neuropeptide expression and social behavior within a single species indicates an additional mediating factor. The purpose of the present comparative study was to investigate social behaviors in naïve mixed-sex pairs of monogamous Peromyscus californicus and polygynous Peromyscus leucopus. We identified substantial inter- and intra-specific variability in the expression of affiliative and agonistic behaviors. Although all P. californicus tested engaged in frequent and prolonged intervals of social contact and rarely engaged in aggressive behaviors, P. leucopus exhibited significant variability in both measures of social behaviors. The naturally occurring differences in social behavior displayed by P. leucopus vary across the estrous cycle, and correspond to hypothalamic oxytocin, as well as circulating oxytocin and glucocorticoid concentrations. These results provide evidence for a rhythm in social behavior across the estrous cycle in polygynous, but not monogamous, Peromyscus species.     

A genetic map of Peromyscus with chromosomal assignment of linkage groups (a Peromyscus genetic map)

The rodent genus Peromyscus is the most numerous and species-rich mammalian group in North America. The naturally occurring diversity within this genus allows opportunities to investigate the genetic basis of adaptation, monogamy, behavioral and physiological phenotypes, growth control, genomic imprinting, and disease processes. Increased genomic resources including a high quality genetic map are needed to capitalize on these opportunities. We produced interspecific hybrids between the prairie deer mouse (P. maniculatus bairdii) and the oldfield mouse (P. polionotus) and scored meiotic recombination events in backcross progeny. A genetic map was constructed by genotyping of backcross progeny at 185 gene-based and 155 microsatellite markers representing all autosomes and the X-chromosome. Comparison of the constructed genetic map with the molecular maps of Mus and Rattus and consideration of previous results from interspecific reciprocal whole chromosome painting allowed most linkage groups to be unambiguously assigned to specific Peromyscus chromosomes. Based on genomic comparisons, this Peromyscus genetic map covers ~83 % of the Rattus genome and 79 % of the Mus genome. This map supports previous results that the Peromyscus genome is more similar to Rattus than Mus. For example, coverage of the 20 Rattus autosomes and the X-chromosome is accomplished with only 28 segments of the Peromyscus map, but coverage of the 19 Mus autosomes and the X-chromosome requires 40 chromosomal segments of the Peromyscus map. Furthermore, a single Peromyscus linkage group corresponds to about 91 % of the rat and only 76 % of the mouse X-chromosomes.     

Patterns of parental care in two cricetid rodents, Onychomys torridus and Peromyscus leucopus

Daily observations were made of the maternal and paternal behaviour of Onychomys torridus and Peromyscus leucopus in laboratory cages. In both species, the females spent more time in the nest area with the young and groomed the young more frequently than their male partners, but the males played a surprisingly active role in nest attendance. Paternal nest attendance was more frequent in O. torridus males than in P. leucopus males. Onychomys males were also more active in grooming the young than Peromyscus males. These species-specific patterns of parental care are discussed in relation to the behavioural and ecological characteristics of Onychomys and Peromyscus.     

Experiments on nest-building behaviour in Peromyscus (Rodentia: Cricetinae)

Previous studies reflect conflicting views on the relative importance of major climatic factors and microhabitat in selection for nest-building behaviour in the genus Peromyscus. In my study, populations of the leucopus species group (P. leucopus and P. gossypinus) from Illinois, Mississippi, and Florida were found not to differ consistently. Populations of P. polionotus, a burrow-nesting form, from Mississippi and Florida scored lower on tests designed to measure nest-building tendency than members of the other two species. I conclude that the evolution of nest-building behaviour in this genus was influenced more by microhabitat than by differences in climate.     

The Good,the Bad,and the Ugly: Agonistic Behaviour in Juvenile Crocodilians

We examined agonistic behaviour in seven species of hatchling and juvenile crocodilians held in small groups (N = 4) under similar laboratory conditions. Agonistic interactions occurred in all seven species, typically involved two individuals, were short in duration (5–15 seconds), and occurred between 1600–2200 h in open water. The nature and extent of agonistic interactions, the behaviours displayed, and the level of conspecific tolerance varied among species. Discrete postures, non-contact and contact movements are described. Three of these were species-specific: push downs by C. johnstoni; inflated tail sweeping by C. novaeguineae; and, side head striking combined with tail wagging by C. porosus. The two long-snouted species (C. johnstoni and G. gangeticus) avoided contact involving the head and often raised the head up out of the way during agonistic interactions. Several behaviours not associated with aggression are also described, including snout rubbing, raising the head up high while at rest, and the use of vocalizations. The two most aggressive species (C. porosus, C. novaeguineae) appeared to form dominance hierarchies, whereas the less aggressive species did not. Interspecific differences in agonistic behaviour may reflect evolutionary divergence associated with morphology, ecology, general life history and responses to interspecific conflict in areas where multiple species have co-existed. Understanding species-specific traits in agonistic behaviour and social tolerance has implications for the controlled raising of different species of hatchlings for conservation, management or production purposes.     

Maternal aggression as a deterrent to infanticide in Peromyscus leucopus and P. maniculatus

Adult male and female white-footed mice (Peromyscus leucopus) and deermice (P. maniculatus) from sympatric populations commit infanticide on neonates of either species. A laboratory experiment was conducted to determine whether aggression in maternal females could effectively deter infanticidal intruders. Females of both species exhibited post-partum aggression and dominated intruders of either sex or species in 83 of 88 trials. In the absence of the mother, neonates were attacked by intruders in 82 out of 84 trials. Maternal females were considerably more aggressive than anoestrous females. The implications for female territorially as a mechanism to prevent infanticide are discussed.     

Dynamic neuromodulation of aggression by vasotocin: influence of social context and social phenotype in territorial songbirds

The homologous neuropeptides vasotocin (VT) and vasopressin (VP) influence agonistic behaviours across many taxa, but peptide–behaviour relationships are complex and purportedly species-specific. Putative species-specific effects in songbirds are confounded with context, however, such that territorial species have been tested only in resident–intruder paradigms and gregarious species have been tested only in a mate competition paradigm. Using the territorial violet-eared waxbill (Estrildidae: Uraeginthus granatina), we now show that a V_1a receptor antagonist reduces male aggression during mate competition (as in gregarious finches), but does not affect resident–intruder aggression in dominant males. However, the V_1a antagonist disinhibits aggression in less aggressive (typically subordinate) males. These results are consistent with recent data on the activation of different VT cell groups during positive and negative social interactions. Thus, VT influences aggression similarly across territorial and gregarious species, but in context- and phenotype-specific ways that probably reflect the differential activation of discrete VT cell groups.     

Variation in aggressive behaviour in the poeciliid fish Brachyrhaphis episcopi: Population and sex differences

Aggression is often positively correlated with other behavioural traits such as boldness and activity levels. Comparisons across populations can help to determine factors that promote the evolution of such traits. We quantified these behaviours by testing the responses of wild-caught poeciliid fish, Brachyrhaphis episcopi, to mirror image stimuli. This species occurs in populations that experience either high or low levels of predation pressure. Previous studies have shown that B. episcopi from low predation environments are less bold than those that occur with many predators. We therefore predicted that fish from high predation populations would be more aggressive and more active than fish from low predation populations. However, we found the opposite - low predation fish approached a mirror and a novel object more frequently than high predation fish suggesting that ‘boldness’ and aggression were higher in low predation populations, and that population-level boldness measures may vary depending on context. When tested individually, low predation fish inspected their mirror image more frequently. Females, but not males, from low predation sites were also more aggressive towards their mirror image. Variation in female aggression may be driven by a trade-off between food availability and predation risk. This suggests that the relationship between aggression and boldness has been shaped by adaptation to environmental conditions, and not genetic constraints.     

Variation in steroid hormone levels among Caribbean Anolis lizards: Endocrine system convergence?

Variation in aggression among species can be due to a number of proximate and ultimate factors, leading to patterns of divergent and convergent evolution of behavior among even closely related species. Caribbean Anolis lizards are well known for their convergence in microhabitat use and morphology, but they also display marked convergence in social behavior and patterns of aggression. We studied 18 Anolis species across six ecomorphs on four different Caribbean islands to test four main hypotheses. We hypothesized that species differences in aggression would be due to species differences in circulating testosterone (T), a steroid hormone implicated in numerous studies across vertebrate taxa as a primary determinant of social behavior; more aggressive species were expected to have higher baseline concentrations of T and corticosterone. We further hypothesized that low-T species would increase T and corticosterone levels during a social challenge. Within three of the four island assemblages studied we found differences in T levels among species within an island that differ in aggression, but in the opposite pattern than predicted: more aggressive species had lower baseline T than the least aggressive species. The fourth island, Puerto Rico, showed the pattern of baseline T levels among species we predicted. There were no patterns of corticosterone levels among species or ecomorphs. One of the two species tested increased T in response to a social challenge, but neither species elevated corticosterone. Our results suggest that it is possible for similarities in aggression among closely related species to evolve via different proximate mechanisms.     

Response to cecropia cocoons of Mus musculus and two species of Peromyscus

Summary In rural areas cocoons of overwintering Hyalophora cecropia spum close to the ground are opened and the pupae eaten by small mammals, but in urban areas, where cecropia populations are much larger, the cocoons are almost never opened by mammals. Peromyscus leucopus noveboracensis and P. maniculatus bairdii are abundant in rural areas, but are largely replaced by Mus musculus in urban areas. In laboratory experiments P. l. noveboracensis invariably opened cecropia cocoons and ate the pupae. P. m. bairdii were slower to open cecropia cocoons and two of twelve did not open one at all. M. musculus, on the other hand, never opened cecropia cocoons although they gnawed the silk and ate uncovered pupae. Cocoons opened in the laboratory by the two species of Peromyscus cannot be distinguished from each other or from cocoons opened in the field.Part of the Ph. D. dissertation presented by the first author to the Department of Entomology, University of Illinois. This investigation was supported in part by PHS Training Grant no. 2-T01-GM 01076 from General Medical Sciences.     

Estrogen Receptor Alpha Distribution and Expression in the Social Neural Network of Monogamous and Polygynous Peromyscus

In microtine and dwarf hamsters low levels of estrogen receptor alpha (ERα) in the bed nucleus of the stria terminalis (BST) and medial amygdala (MeA) play a critical role in the expression of social monogamy in males, which is characterized by high levels of affiliation and low levels of aggression. In contrast, monogamous Peromyscus males display high levels of aggression and affiliative behavior with high levels of testosterone and aromatase activity. Suggesting the hypothesis that in Peromyscus ERα expression will be positively correlated with high levels of male prosocial behavior and aggression. ERα expression was compared within the social neural network, including the posterior medial BST, MeA posterodorsal, medial preoptic area (MPOA), ventromedial hypothalamus (VMH), and arcuate nucleus in two monogamous species, P. californicus and P. polionotus, and two polygynous species, P. leucopus and P. maniculatus. The results supported the prediction, with male P. polionotus and P. californicus expressing higher levels of ERα in the BST than their polygynous counter parts, and ERα expression was sexually dimorphic in the polygynous species, with females expressing significantly more than males in the BST in both polygynous species and in the MeA in P. leucopus. Peromyscus ERα expression also differed from rats, mice and microtines as in neither the MPOA nor the VMH was ERα sexually dimorphic. The results supported the hypothesis that higher levels of ERα are associated with monogamy in Peromyscus and that differential expression of ERα occurs in the same regions of the brains regardless of whether high or low expression is associated with social monogamy. Also discussed are possible mechanisms regulating this differential relationship.     

Lack of Evidence for the Prior Residence Effect in the Allegheny Mountain Dusky Salamander (Desmognathus ochrophaeus)

Territorial disputes are frequently settled by an advantage afforded to one of the contestants by asymmetries such as size difference, strength and motivation. Allegheny Mountain Dusky Salamanders (Desmognathus ochrophaeus) are reported to defend cover objects, a form of territorial behaviour. We conducted an experiment to determine whether or not adult salamanders of this species exhibit prior residence effect during staged encounters involving size‐matched, same sex conspecifics (i.e. does familiarity with a territory predict successful defence?). We tested 154 adult salamanders (72 female, 82 male) in reciprocal trials in which each animal acted as a resident and as an intruder. We recorded multiple agonistic behaviours including: front‐trunk raised, all‐trunk raised, nudge, bite, bite‐and‐hold and jaw‐lock. We assigned these behaviours scaled point values and calculated an index of aggression for each animal as a resident and as an intruder. We found that in same sex trials, males were significantly more aggressive than females. Although D. ochrophaeus exhibited stereotypical, agonistic behaviours similar to those reported for Plethodon, unlike Plethodon the outcomes of symmetrical social encounters were not influenced by residential status. Prior residence is documented to be a major determinant of territorial disputes among diverse animal taxa, including salamanders. However, our research suggests that the phenomenon is not universal and may depend on qualities of the microhabitat in which a species has evolved.     

Trade-off between growth rate and aggression in juvenile coho salmon, Oncorhynchus kisutch

In juvenile salmon and trout, there seems to be a positive phenotypic correlation between individual aggression level and growth rate. Aggressive fish are dominant, and they obtain and defend territories, giving them access to good feeding sites. Being aggressive may increase predation risk, and may also carry costs such as increased metabolic demand, with effects on growth. To test the hypothesis that there is a trade-off between individual growth rate and aggression, we mated 12 female coho salmon with two unique males each, creating 24 full-sibling families. Growth of individually marked fish from each family was estimated in a situation where food could not be monopolized. Thereafter, individual fish were tested for mirror-elicited agonistic behaviour. We found significant variation between families in early growth rate, with a high heritability (1.04). There was also significant between-family variation in agonistic behaviour, but activity was generally low and heritability was low (0.25) and not significant. Growth rate and agonistic behaviour were negatively correlated. These results imply that aggressive behaviour has an energetic cost. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

QUANTITATIVE GENETICS OF MORPHOLOGICAL DIFFERENTIATION IN PEROMYSCUS. I. TESTS OF THE HOMOGENEITY OF GENETIC COVARIANCE STRUCTURE AMONG SPECIES AND SUBSPECIES

Phenotypic and additive genetic covariance matrices were estimated for 15 morphometric characters in three species and subspecies of Peromyscus. Univariate and multivariate ANOVAs indicate these groups are highly diverged in all characters, P. leucopus having the largest body size, P. maniculatus bairdii the smallest, and P. maniculatus nebrascensis being intermediate. Comparing the structure of P and G within each taxon revealed significant similarities in all three cases. This proportionality was strong enough to justify using P in the place of G to analyze evolutionary processes using quantitative genetic models when G can not be estimated, as in fossil material. However, the similarity between genetic and phenotypic covariance structures is sufficiently low that estimates of the genetic parameters should be used when possible. The additive genetic covariance matrices were compared to examine the assumption that they remain constant during evolution, an assumption which underlies many applications of quantitative-genetic models. While matrix permutation tests indicated statistically significant proportionality between the genetic covariance structures of the two P. maniculatus subspecies, there is no evidence of significant genetic structural similarity between species. This result suggests that the assumption of constant genetic covariance structure may be valid only within species. (It does not, however, necessarily imply a causal relationship between speciation and heterogeneity of genetic covariance structures.) The low matrix correlation for the two P. maniculatus subspecies' genetic covariance matrices indicates G may not be functionally constant, even within species. The lack of similarity observed here may be due partly to sampling variation.     

Aggressive behaviour of female prairie deer mice in laboratory populations

Prairie deer mice (Peromyscus maniculatus bairdii), living in asymptotic laboratory populations established two years earlier, were observed for agonistic responses to conspecific intruders. In the first experiment, intruders of six age-sex classes were placed into 10 of the populations for 10 min. The sex of the intruder did not influence the behaviour of the residents, but juveniles elicited more aggression than did adults. A second experiment revealed that female residents were responsible for almost all of the attacks upon juveniles. Experiment 3, in which the responses of pairs of deer mice to juvenile intruders were recorded, demonstrated that the aggressiveness of a female was enhanced by the presence of a male. In the final experiment, females were observed to be highly aggressive during the first few days after giving birth. The aggressive behaviour of the female deer mouse may have greater significance for population dynamics than that of the male.     

Interference with ritualized threat behaviour in Cichlasoma nigrofasciatum

According to ethological theory, ritualized threat behaviour functions to prevent overt aggression. This prediction was tested in twenty-three pairs of male Cichalasoma nigrofasciatum. Pairs prevented from giving frontal displays by surgically restrained gill covers showed significantly less mouth fighting than sham operates. Pairs prevented from giving frontals and impaired in delivering tail beats because of separated caudal-fin rays showed intermediate aggressive behaviour. Experimental animals in both groups fought and frequently became dominant when paired with sham operates. It was concluded that threat behaviour in C. nigrofasciatum increases subsequent aggressive behaviours both quantitatively and qualitatively. It is suggested that ethological theory has identified the effects of ritualized aggression as a complex behavioural sequence ending in submissive behaviour with that of its first phase alone.     

Aggression by the damselfish Dascyllus aruanus L. Towards conspecifics and heterospecifics

Field experiments were conducted to demonstrate species recognition in Dascyllus aruanus. Aggression was used as a criterion for recognition. Free-living fish were presented with live stimuli in a choice situation where visual cues could be isolated from other cues. The stimuli were conspecific and heterospecific fish. Practically all the responses were aggressive. Aggression towards D. aruanus and Dascyllus marginatus was similar in its intensity, and higher than towards Dascyllus trimaculatus. Aggression towards Amphiprion bicinctus was negligible. Elimination of all but visual cues resulted in a decline in attack rate without changing attack preference. The high level of interspecific aggression limits the use of aggression as an indicator of species recognition under the presented experimental situation.     

Allelopathic effects of the Baltic cyanobacteria Nodularia spumdigena, Aphanizomenon flos-aquae and Anabaena lemmermannii on algal monocultures

Allelopathy, the release of extracellular compounds that inhibit the growth of other microorganisms, may be one factor contributing to the formation and/or maintenance of cyanobacterial blooms. We investigated the allelopathic effects of three cyanobacterial species (Nodularia spumigena, Aphanizomenon flos-aquae and Anabaena lemmermannii) that frequently form mass-occurrences in the Baltic Sea. We exposed monocultures of three phytoplankton species (Thalassiosira weissflogii, Rhodomonas sp. and Prymnesium parvum) to cell-free filtrates of the three cyanobacteria, and quantified allelopathic effects with cell counts. We also investigated the role of the growth phase of cyanobacteria in their allelopathy, by comparing the effects of an exponential and a stationary phase culture of N. spumigena. All tested cyanobacteria inhibited the growth of Rhodomonas sp., but none of them affected P. parvum. The effects on T. weissflogii were more variable, and they were amplified by repeated filtrate additions compared to a single filtrate addition. N. spumigena was more allelopathic in exponential than in stationary growth phase, whereas the culture filtrate was more hepatotoxic in stationary phase. Hepatotoxins were thus probably not involved in the allelopathic effects, which is also indicated by the allelopathic properties of the non-toxic A. flos-aquae and A. lemmermannii. The results demonstrate that the common Baltic cyanobacteria affect some coexisting phytoplankton species negatively. Allelopathy may therefore play a role in interspecific competition and contribute to cyanobacterial bloom maintenance.     

Vocalizations of Belding's ground squirrels (Spermophilus beldingi)

Vocalizations of Belding's ground squirrels (Spermophilus beldingi) were recorded during the summer of 1982 near Tioga Pass in the central Sierra Nevada of California. Sonagrams were made and call parameters were measured. Discriminant function analyses revealed that multiple-note calls (‘trills’) differed acoustically depending on whether they occurred in response to a predator, or were given by males following copulations. The post-copulatory trills of males were individually distinctive. Among anti-predator trills there was no evidence of predator-specificity within the narrow range of predators tested: trills given to two species of (stuffed) weasels (Mustela), to dogs and to humans were statistically indistinguishable. Sonagrams of trills occurring in agonistic contexts suggest that a third general category of trills may exist, but agonistic trills were more variable than either anti-predator or post-copulatory trills. The ground squirrels also gave single-note calls in the three contexts described above, either repetitively (‘chirps’) or singly (‘whistles’). Neither chirps nor whistles encoded any obvious situation-specific information, except that whistles were typically associated with rapidly-moving predators, usually raptors. The post-copulatory chirps of males were individually distinctive. Vocalizations of Belding's ground squirrels may not vary among contexts as much as do the analogous calls of California ground squirrels (S. beecheyi).     

Behaviours of collared and white-lipped peccaries (Tayassu tajacu andT. pecari) in relation to sexual receptivity of the female

Changes in behaviours of the two peccary species,Tayassu tajacu Linnaeus, 1758 andT. pecari Link, 1795 between non-receptive and receptive periods were followed by presenting females to males daily for 15 minutes. InT. tajacu, the rank order of behaviours, similar in both sexes during the non-receptive period, differs during receptivity. Contact behaviours decrease in males, whereas sexual ones progress. The same tendency appears in females. Inhibited bites replace markings of partner as the most common behaviour in both sexes. InT. pecari, the rank order of behaviours always differs between sexes. When females become receptive, the differences from the non-receptive period are neither numerous nor significant. The most common behaviour of males, previously markings of partner, becomes mounts, whereas in females agonistic behaviours reinforce their dominance. In this species, the only behaviours that increase are those leading directly to copulation or those of an agonistic nature. In both species, females show more agonistic behaviours than males (mainly inhibited bites inT. tajacu, truly aggressive ones inT. pecari). When females are receptive, males ofT. pecari become less active, contrary toT. tajacu where both sexes double their activity. InT. tajacu, most behaviours vary significantly in relation to the progesterone level, contrary to the other species. These pecularities appear correlated to herd composition and organisation.