Adolescent social environment shapes sexual and aggressive behaviour of adult male zebra finches (Taeniopygia guttata)

Adolescence is the pivotal transitional phase during which animals become sexually and socially mature and acquire the skills to cope with a variety of environmental challenges on their own. We investigated in a bird species, the zebra finch, how the social environment experienced during this period influences their behaviour in a sexual context. Zebra finches were kept in pairs (male–female or male–male) or larger mixed-sex groups (three males and three females) during adolescence and the long-term consequences were studied on courtship behaviour, aggressiveness and attractiveness in 42 males. To investigate the stability of the observed effects over time, all behavioural tests were repeated approximately 4 months after the initial recordings. Males that grew up with a single female showed the most intense courtship and highest aggressiveness and were most attractive to females, while group-reared males had the lowest courtship and aggressiveness and were the least attractive. The observed differences in courtship and aggressiveness were stable, while the differences in attractiveness disappeared over time. These findings are very similar to earlier studies on guinea pigs, indicating that the observed effects represent a general phenomenon, not restricted to mammals with a similar function and presumably also similar underlying mechanisms.     

Extra-pair paternity and intraspecific brood parasitism in wild zebra finches Taeniopygia guttata,revealed by DNA fingerprinting

Summary The frequency of extra-pair parentage in a wild population of zebra finches Taeniopygia guttata was examined by DNA fingerprinting. A total of 25 families, comprising 16 pairs of parents and 92 offspring (in broods of 1 to 6) were examined. Ten cases of extra-pair parentage, presumed to constitute intraspecific brood parasitism, were detected (10.9% of offspring or 36% of broods), including one possible instance of quasi-parasitism (parasitism by a female fertilized by the male nest owner). The average number of parasitic eggs per clutch detected by fingerprinting was 1.10±0.32 SD, very similar to the one egg difference in average clutch size between parasitised (6.0±0.82) and unparasitised nests (5.0±0.95). Two cases of extra-pair paternity (EPP) were detected among 82 offspring whose maternity was confirmed: 2.4% of offspring, or 8% of broods. In both cases EPP accounted for only a single offspring within a brood. Behavioural observations show that EPP occurs through extra-pair copulation rather than rapid mate switching. The results are discussed in the light of what is known about the fertile period and sperm precedence patterns in this species. Offprint requests to: T.R. Birkhead     

Developmental stress affects the attractiveness of male song and female choice in the zebra finch (Taeniopygia guttata)

Developmental stress has recently been shown to have adverse effects upon adult male song structure in birds, which may well act as an honest signal of male quality to discriminating females. However, it still remains to be shown if females can discriminate between the songs of stressed and non-stressed males. Here we use a novel experimental design using an active choice paradigm to investigate preferences in captive female zebra finches (Taeniopygia guttata). Nine females were exposed to ten pairs of songs by previously stressed and non-stressed birds that had learned their song from the same tutor. Song pairs differed significantly in terms of song complexity, with songs of stressed males exhibiting lower numbers of syllables and fewer different syllables in a phrase. Song rate and peak frequency did not differ between stressed and non-stressed males. Females showed a significant preference for non-stressed songs in terms of directed perching activity and time spent on perches. Our results therefore indicate that developmental stress affects not only the structure of male song, but that such structural differences are biologically relevant to female mate choice decisions.     

Family-related differences in social foraging tactic use in the zebra finch (Taeniopygia guttata)

When animals forage in groups, they can search for food themselves (producer tactic), or they can search for opportunities to exploit the food discoveries of others (scrounger tactic). Both theoretical and empirical work have shown that group-level use of these alternative tactics is influenced by environmental conditions including group size and food distribution, and individual tactic use can be influenced by several measures of individual state, including body condition. Because body condition has been shown to be heritable for various species, social foraging tactics may also be heritable. We looked for evidence of heritability in social foraging tactic use in the zebra finch (Taeniopygia guttata) by testing whether: (1) natural variation in body condition correlates with tactic use, (2) there are family-related differences in body condition, and (3) there are family-related differences in observed tactic use. Tactic use in the zebra finch was significantly related to body condition; individuals with lower body condition scores had a significantly higher use of the scrounger tactic as predicted from variance-sensitive producer–scrounger models. Body-condition scores differed significantly between families, suggesting that this aspect of individual state may have a heritable component. Finally, we recorded significant family-related differences in the use of producer and scrounger alternatives. These results are consistent with heritability in observed tactic use resulting from an inheritance of individual state, in this case body condition, which itself influences tactic use. Understanding how and why individuals differ in their use of alternative tactics is fundamental as it may provide important insights into inter-individual variation in fitness.     

Developmental stress impairs song complexity but not learning accuracy in non-domesticated zebra finches (<Emphasis Type="Italic">Taeniopygia guttata</Emphasis>)

Food restrictions early in life can have adverse effects on the development of adult avian song structure. Nutritional deficiencies during brain development are thought to impair the growth of neural circuits responsible for learning and production of song in adulthood. Thus, the quality of song may reflect the quality of the singer due to the costs associated with neural development early in life. Recent investigations have focused on domesticated laboratory strains of zebra finches where early dietary deficiencies have significantly reduced the complexity of song and its sexual attractiveness. Domesticated zebra finches may be more sensitive to the early effects of moderate under-nutrition on song complexity than their non-domesticated counterparts. In an aviary experiment with non-domesticated zebra finch stock, we found that song complexity when measured by a linear combination of six variables was reduced in food-restricted birds, with syllable rate and maximum syllable frequency as the principal variables affected. The restriction had no effect on learning accuracy when song phrases of experimental birds were compared to those of their fathers.This result demonstrates that early nutrition may differentially affect the development of neural processes that influence learning accuracy and song complexity. While the finding of negative effects of dietary restriction on song complexity is robust for zebra finches and is not an artefact of domestication, it does not explain why some nutritionally stressed populations of wild zebra finches have more complex songs than those from other regions of Australia characterised by greater food availability.     

Reproductive status influences group size and persistence of bonds in male plains zebra (<Emphasis Type="Italic">Equus burchelli</Emphasis>)

Animal groups arise from individuals’ choices about the number, characteristics, and identity of associates. Individuals make these choices to gain benefits from their associations. As the needs of an individual change with its phenotype, so too we expect the nature of its associations to vary. In this paper, we investigate how the social priorities of male plains zebra (Equus burchelli) depend on reproductive state. An adult male is either a bachelor, and lacking mating access, or a stallion defending a harem. Multiple harems and bachelor males aggregate in larger herds. Herds frequently split and merge, affording males opportunities to change associates. Over a 4-year period, we sampled the herd associations in a population of 500–700 zebras. To isolate the effects of reproductive state on male social behavior, we account for potential confounding factors: changes in population size, grouping tendencies, and sampling intensity. We develop a generally applicable permutation procedure, which allows us to test the null hypothesis that social behavior is independent of male status. Averaging over all individuals in the population, we find that a typical bachelor is found in herds containing significantly more adults, bachelors, and stallions than the herds of a typical stallion. Further, bachelors’ bonds with each other are more persistent over time than those among stallions. These results suggest that bachelors form cohesive cliques, in which we may expect cooperative behaviors to develop. Stallion–stallion associations are more diffuse, and less conducive to long-term cooperation. This contribution is part of the special issue “Social Networks: new perspectives” (Guest Editors: J. Krause, D. Lusseau and R. James).     

Testosterone and the allocation of reproductive effort in male house finches (Carpodacus mexicanus)

Testosterone has been proposed to serve as the mediator that controls the relative effort that an individual male bird will devote to mating effort versus parental effort. Here, we demonstrate a testosterone-influenced trade-off between parental and mating efforts in male house finches. Male house finches with experimentally elevated testosterone fed nestlings at a significantly lower rate, but sang at a higher rate than males without manipulated testosterone levels. Females mated to testosterone-implanted males fed nestlings at a significantly higher rate than females mated to males without testosterone implants, resulting in similar feeding rates for both treated and untreated pairs. The effects of testosterone on male house finches, however, were not as dramatic as the effects of testosterone observed in some other socially monogamous species of birds. Because extra-pair copulations are uncommon in house finches and males provide substantial amounts of parental care, these more modest effects may be due to differences in how the allocation of reproductive effort affects the costs and benefits of different reproductive behaviors. Received: 6 June 2000 / Accepted: 17 July 2000     

Exaggerated male eye span influences contest outcome in stalk-eyed flies (Diopsidae)

Evolution of male weapons or status signals has been hypothesized to precede evolution of female mating preferences for those traits. We used staged male fights among three species of Malaysian stalk-eyed flies (Diptera: Diopsidae) to determine if elongated eye span, which is preferred by females in two sexually dimorphic species, influences contest outcome. Extreme sexual dimorphism, with large males possessing longer eye span than females, is shared by Cyrtodiopsis whitei and C. dalmanni. In contrast, C. quinqueguttata exhibits a more ancestral condition – short, sexually monomorphic eye stalks. Videotape analysis of 20-min paired contests revealed that males with larger eye span and body size won more fights in the dimorphic, but not monomorphic, species. To determine if males from the dimorphic species use eye span directly to resolve contests, we competed male C. dalmanni from lines that had undergone artificial selection for 30 generations to increase or decrease eye span. We found that eye span, independently of body size, determines contest outcome in selected-line males. Furthermore, in both dimorphic species, the average encounter duration declined as the eye span difference between contestants increased, as expected if males use eye span to assess opponent size. The number of encounters also increased with age in dimorphic, but not monomorphic, species. Selected-line males did not differ from outbred males in either fight duration or number of encounters. We conclude that exaggerated male eye stalks evolved to influence both competitive interactions and female mating preferences in these spectacular flies. Received: 20 July 1998 / Received in revised form: 2 February 1999 / Accepted: 12 March 1999     

Social cohesion and foraging decrease with group size in fallow deer (Dama dama)

We studied the impact of group size on foraging behaviour and level of movement synchronisation among female herdmates of a fallow deer population in Central Italy. Both proportion of foraging events and movement synchronisation decreased with increasing group size. The proportion of foraging events was higher for animals on the edge of the group than for deer in the centre of the group; hence, there appears to be a trade-off between protection against predators and foraging interference, both of which decrease from the centre to the periphery of the group. This is the first time this type of behaviour has been recorded for wild ungulates. As expected, we also found that the movement of peripheral animals was less synchronised than that of central animals. Consequently, peripheral animals may lose contact with their herdmates and split off the group. We conclude that social inequalities may lead to conflicting requirements among group members and instability of large groups. Movement synchronisation (as a function of group size) appears to interact with habitat openness to produce variations of group size (which appear to be adaptive for individuals) as an emergent property of these aggregations.     

Endocrine influences on parental care during a short breeding season: testosterone and male parental care in Lapland longspurs (Calcarius lapponicus)

In males of socially monogamous birds, plasma testosterone (T) typically declines to low levels during the parental phase. Studies on multiple-brooded species indicate that high T may be incompatible with high-quality paternal care. The length of the breeding season may affect the costs and benefits of high T and its effect on paternal care. We studied the effect of experimentally elevated T on paternal care in a single-brooded species with a short breeding season, the Lapland longspur (Calcarius lapponicus). We monitored T levels and parental behavior in 16 males with subcutaneous T implants, 14 males with empty implants, and 14 unimplanted males. We videotaped nests when nestlings were 2–3 days old and again at 4–5 days. T males with 2- to 3-day-old young visited nests and fed young less often than control males, and the mates of the T males compensated with elevated visits and feedings. However, when nestlings were 4–5 days old, T males visited their nests at normal rates – though feeding movements remained below normal – and T females visited and fed at normal rates. Nestling mass and nest success were similar in both groups. Overall, high T suppresses paternal care in Lapland longspur males. The partial improvement of paternal care when nestlings are older, despite high T, may be related to the short 6-week breeding season of this arctic species, and the consequently reduced benefits of sexual behavior late in the breeding season. Received: 2 February 1998 / Accepted after revision: 2 November 1998     

Social relationships in a cooperatively polyandrous group of tamarins (Saguinus fuscicollis)

Summary This paper presents detailed data on the social relationships among the adults, and between the adults and young, of a cooperatively polyandrous saddle-back tamarin (Saguinus fusciollis; Callitrichidae) group studied for one year. Some data are also presented from groups studied in other years. Adult males in the study groups gave more grooming than they received, while the opposite was true for females (e.g. Fig. 1). The two polyandrous males in the main study group were very rarely aggressive to each other, rarely tried to disrupt each others' copulations, groomed each other, and occasionally shared food, suggesting that their relationship was more affiliative than agonistic. Data on grooming (Fig. 2), spatial relationships, and the initiation of copulations suggest that the males of this group, may have been somewhat more responsible than the female for the maintenance of male-female relationships. Both males and females performed all forms of parental care except lactation. In the main study group each of the males groomed the offspring and remained in close proximity to them more than did the female (Figs.3 and 4). These data are compared with existing data on social relationships in bird species that exhibit cooperative polyandry.     

Mating group composition influences somatic costs and activity in rutting dominant male reindeer (<Emphasis Type="Italic">Rangifer tarandus</Emphasis>)

In polygynous species, males devote considerable effort to reproduction during the rut. Both the number of females in the mating group and the ratio of sexually mature males to sexually mature females [adult sex ratio (ASR)] are expected to affect the amount of effort a male devotes to reproductive activities. We predicted the reproductive effort of dominant male reindeer, measured as relative mass loss, proportions of active reproductive behaviors, and frequencies of agonistic behaviors would (1) increase with an increasing number of females in the mating group and eventually level off, and (2) exhibit a dome shape with respect to ASR in the mating group. We tested these predictions using 12 years of data collected from semi-domesticated reindeer in northern Finland. We found a positive relationship between relative mass loss and the mean number of females in the mating group for mature, but not young males. The relationship between the proportion of active reproductive behaviors performed by mature males and the mean number of females in the group was quadratic while agonistic behaviors of mature males increased with the increasing female group size. We also found that active reproductive behaviors decreased with a rising mating group ASR for mature males; whereas, young males performed more agonistic behaviors as group ASR increased. Our results point to age-specific patterns of mass loss and activity during the mating season. They also indicate that both the number of females and ASR in the mating group are important factors in determining the level of reproductive effort of dominant male reindeer.     

Territory ownership and familiarity status affect how much male root voles (Microtus oeconomus) invest in territory defence

Neighbour–stranger discrimination occurs when individuals respond with more aggression to strangers than to territorial neighbours—a phenomenon termed the “dear enemy phenomenon” (DEP). We investigated the DEP with male and female root voles (Microtus oeconomus Pallas 1776) using field dyadic arena tests conducted in enclosures where we could test for the effects of familiarity (familiar versus stranger), ownership (resident versus intruder status) and resource-holding potential (body mass) on territorial behaviours. The results showed that males put more effort into territorial defence than females, and males could discriminate between neighbours and strangers. In males, aggressiveness was influenced by a significant two-way interaction between treatment and ownership. Male residents were more aggressive towards stranger intruders than towards neighbour intruders, while male intruders were less aggressive towards stranger residents than towards neighbour residents. In females, neither treatment nor ownership status had a significant effect on aggressiveness. Familiar males performed more social behaviours but less non-social behaviours than stranger males. Furthermore, there was a clear dominance hierarchy between residents and intruders in stranger dyads, with the male territory holders dominating the intruder in pairwise interactions. To our knowledge, these results demonstrate for the first time DEP in a small mammal with a known pedigree and present the first evidence for “prior resident advantage” in voles. We argue that both ownership status and familiarity status affect how much an individual invests in territory defence. The benefits of neighbour–stranger discrimination for male root voles and the absence of neighbour–stranger discrimination in female root voles are discussed.     

Males are selective too: mating, but not courtship, with sequential females influences choosiness in male field crickets (Gryllus bimaculatus)

Mate choice experiments have generally focused on female choice; few have considered that males can also be selective. We examined courtship in male field crickets sequentially introduced to four females of differing size. Large (L) and small (S) females were introduced in order of either LSLS or SLSL. We demonstrate that naive males invest equally (courtship effort) in the first female they meet, regardless of her size, but show greater courtship effort when they subsequently encounter large compared with small females. Moreover, we demonstrate that males show this discriminatory behavior when they are permitted to mate with females (i.e. use a spermatophore) but are less choosy when the female is removed before spermatophore transfer.     

Dominions and desert clickers (Orthoptera:Acrididae): influences of resources and male signaling on female settlement patterns

Summary Previous field work on the grasshopper Ligurotettix coquilletti revealed that females were not evenly distributed among male mating territories, Larrea tridentata (creosote) bushes, but were clustered at particular locations. These sites generally harbored several signaling males simultaneously and also possessed foliage preferred by the insects as a food source, this preference being based on the relative concentrations of various extra-foliar compounds. The clustering of females, therefore, could result from a preference for specific bushes because of the resources (i.e., food) available there and/or an orientation to groups of males per se. Here, we present the results of 3 field experiments in which we controlled the spatial distribution and intensity of male signals using a computer-operated system of loudspeakers and monitored the movement of individually marked females released in the study area. When male song was identical at high and low quality territories (all having single loudspeakers), females still aggregated at the high quality sites, indicating that variability in host plant quality alone may be sufficient to promote a skewed distribution of females. Among high quality territories, females did not discriminate between sites with one versus three loudspeakers (all broadcasting the same signal), but displayed a strong preference for sites (all having single loudspeakers) with a high intensity signal over a low intensity one. Field measurements showed that the songs of grouped males were more intense than those of lone males, implying that the signaling of grouped males may have enhanced the settlement of females at the bushes harboring male groups above and beyond that influenced by territory quality alone. We conclude that female attraction to host plants is influenced primarily by male signaling, whereas their subsequent retention is more dependent on territory quality. An experiment on male settlement failed to show an aggregative tendency, suggesting that male groups form through the passive accumulation of individuals at high quality sites.     

Effects of experience and avpr1a microsatellite length on parental care in male prairie voles (Microtus ochrogaster)

Pair-bonded males often make substantial contributions to the care of their offspring. Male parental behavior may be affected by a range of factors, including previous experience (parental or alloparental), genetic influences, and contributions by the female partner. Previous studies have shown that a microsatellite polymorphism in the regulatory region of the avpr1a gene influences aspects of paternal behavior in male prairie voles (Microtus ochrogaster). Specifically, males with longer avpr1a microsatellites groomed offspring more than did males with shorter avpr1a microsatellites. Previous experience with alloparental care also appears to influence subsequent paternal care in prairie voles. We investigated the influence of avpr1a microsatellite length and previous parental experience on paternal behavior in prairie voles two generations from the field and specially bred to exaggerate differences in avpr1a microsatellite length. We found that avpr1a microsatellite length alone did not affect any of the paternal behaviors that we measured. In contrast, males differed in parental behavior between first and second litters. Regardless of avpr1a microsatellite length, males licked/groomed the second litter less, and retrieved pups more quickly during the second compared to the first litter. Our results show that previous paternal experience may play a more important role than the length of the microsatellite in the regulatory region of the avpr1a gene in influencing paternal care.     

Escalating fights for rank-order position between male swordtails (Xiphophorus helleri): Effects of prior rank-order experience and information transfer

Summary A previous hypothesis which we originally based on standardized mirror tests was examined. It stated that subordinate males from socially stabilized groups, when confronted with a strange male of similar fighting ability, tend to take the offensive; in contrast, dominant males tend to wait and see and to increase their aggressiveness only as far as necessary to counter the aggressive actions of the opponent. 30 highly escalating fights between well matched opponents, either with different or with the same prior rank-order experience, were recorded on video tape and then analysed in detail. Rank-order experience affected neither the escalation level nor the outcome of the fights. However, in the first nonescalated stage of the fights all measures of unilateral aggressive actions were higher in the omega than in the alpha males. This is contrary to expectations based on the theory of social conditioning; nor can it yet be explained by game-theory models. We then discuss why it should pay subordinates to be more offensive and to show higher levels of unilateral aggression than dominants. Some current aspects of game theory are supported by our data: (1) Threat display is a poor predictor of attack and fleeing, and simply informs the opponent that the threatening individual will probably just stay and avoid further escalations. (2) Relative fighting ability is demonstrated during highly-escalated fighting by delivering Fin Grips, the most effective and costly attack pattern. The high energetic costs of Fin Grips can be compensated by reducing the rate of Biting. (3) Probably, the combatants did not transfer information about their intentions, i.e. they concealed their intentions as to what they were going to do next. Contrary to the predictions of game theory, winners and losers showed some differences in Pecking early in the nonescalated stage of the fights, the prospective losers exhibiting more Pecking than the winners.This study was supported by grants from the Deutsche Forschungsgemeinschaft     

A stereoscan electron microscope study of male reproductive characters in the Jaera albifrons group of species (Crustacea: Isopoda)

The male secondary sex characters of Jaera albifrons Leach, Jaera ischiosetosa Forsman, Jaera praehirsuta Forsman and Jaera forsmani Bocquet are described with the Stereoscan electron microscope (S.E.M.). These characters, which are present on the peraeopods, are the only means of identification for these Jaera species which together form the Jaera albifrons group (Isopoda, Asellota). The male praeoperculum (modified, fused, first pair of pleopods) and appendix masculinae (modified endites of the second pair of pleopods) have also been studied with the S.E.M. and possible functions of the various sex characters are discussed. Both the male operculum and appendix masculinae are similar for each species, suggesting that copulation with females of a different species is anatomically possible. The fact that hybrids are rarely collected in ecological investigations is discussed with reference to the present known information. Two methods of copulation for the members of this group have been proposed and these are discussed. A method of sperm transfer along the male operculum is outlined.     

Sperm characteristics associated with different male reproductive tactics in bluegills (Lepomis macrochirus)

We examined the availability and motility of sperm from parental and sneaker male bluegills (Lepomis macrochirus), a colonially nesting sunfish (Family Centrarchidae) with male parental care and a high incidence of cuckoldry by both sneaker and satellite males. We found no differences between sneakers and parentals in length and swimming speed of sperm, or percent and duration of sperm activity. In sneaker milt, however, sperm was almost 50% more concentrated than in parental milt (16.5×10⁶ vs 11.5×10⁶ sperm/μl of milt, respectively). Despite this difference in sperm concentration, stripped ejaculates from sneakers contained almost 400 million fewer sperm (only 32% as many sperm) than those from parentals due to their much smaller stripped ejaculate volumes (only about 19% that of parentals). Thus unless sneakers can compensate by releasing more sperm or gaining closer proximity to eggs at the time of spawning, they may be at a disadvantage with respect to sperm competition. We discuss these results in relation to models for the evolution of alternative reproductive behaviours in this species and suggest that the cuckolders may be making the best of a bad situation. Received: 18 February 2000 / Revised: 23 March 2000 / Accepted: 14 September 2000