Androgen-dependent maternal effects on offspring fitness in zebra finches

There is accumulating evidence that maternal hormones may play a role in offspring sex adjustment, but little is known about the costs of such hormone-mediated mechanisms. Recent studies have reported sex-specific effects of hormones on offspring viability. Specifically, we previously found that elevating the plasma androgen level in mothers results in a male-biased offspring primary sex ratio, but it affects the viability of sons negatively and daughters positively in zebra finches (Taeniopygia guttata; Rutkowska and Cichoń, Anim Behav, 71:1283–1288, 2006). In this study, we studied further fitness consequences of exposure to elevated yolk androgen levels in zebra finches. We measured growth rate and cellular immune response of nestlings that hatched from eggs laid by females injected with testosterone during egg laying and nestlings of unaffected control females. We found that sons of testosterone-treated females grew slower in comparison to sons of control females. The significant interaction between experimental group and offspring sex indicates that sons of testosterone-treated mothers suffered impaired immune responsiveness while daughters seemed to benefit from elevated androgen level in terms of enhanced immune responsiveness. We found no effects of androgens on offspring performance at adulthood—neither fecundity of females nor attractiveness of males was affected. We conclude that the benefits of biasing sex ratio towards males by increasing androgen level in the yolk may be limited due to negative effects on male offspring performance early in life.     

Immunoregulatory activity of different dietary carotenoids in male zebra finches

Summary. Many animals use carotenoid pigments to color their integument and become sexually attractive. These colorants can also serve physiological functions, protecting cells and tissues from oxidative damage as well as stimulating the immune system. Because animals often acquire several different carotenoid pigments from their diet, there is the potential for different carotenoids to exhibit different free-radical-scavenging or immunoenhancing activity. We experimentally tested how two common dietary xanthophylls - lutein and zeaxanthin - may differentially affect the immune system in male zebra finches (Taeniopygia guttata). Male T. guttata derive their red sexual beak colorants from these two carotenoids, and prior studies with this species have shown that lutein and zeaxanthin together boost cell-mediated immunity. We experimentally elevated these two dietary carotenoids separately in two groups of non-breeding zebra finches, but found that lutein-supplemented and zeaxanthin-supplemented males mounted similar cell-mediated immune responses (to phytohaemagglutinin, or PHA). Although zeaxanthin is a more conjugated carotenoid than lutein and has the potential to be a more potent antioxidant, our study suggests that such a subtle structural difference between these two biochemicals does not differentially affect immune performance in this songbird.     

Manipulating the perceived opportunity to cheat: an experimental test of the active roles of male and female zebra finches in mate guarding behavior

Birds are commonly sexually promiscuous, which can lead to conflict between the sexes and the evolution of paternity assurance strategies, such as mate guarding. Adaptive explanations for mate guarding have tended to focus on fitness consequences for males, but mate guarding and participation in being guarded is also likely adaptive for females in certain contexts. To better understand the adaptive explanations for mate guarding as well as the observed variation in paternity patterns, it is necessary to explore the relative costs and benefits of guarding (and being guarded) from both the male and female perspective. To investigate these costs and benefits, we conducted an experiment with the Australian zebra finch (Teniopygia guttata) in which we independently varied the perceived opportunity for each member of a captive breeding pair to engage in extra-pair copulation (EPC) solicitation behavior; as an individual’s EPC opportunity increased, the partner’s EPC opportunity remained constant. Our results indicate that, for males, mate guarding intensity increases when their female’s EPC opportunity increases but decreases when their own (i.e., male) EPC opportunity increases. We did not find evidence of flexible female guarding behavior, but we found that females do not evade their partners more as female EPC opportunity increases.     

Social feedback and attractiveness in zebra finches

The attractiveness of an individual (i.e. its ability to arouse interest in a potential mate) has important implications for its reproductive success. However, attractiveness is not a fixed trait. Previous work has shown that male birds can adjust the intensity of their courtship display in response to variation in female behaviour, but little is known about how males adjust their behaviour during mate choice in response to social feedback about their own attractiveness independent of their intrinsic quality. Such information may help to maximize the potential mating success of males. Here, we provide experimental evidence that the amount of attention given by male zebra finches to females is dependent upon the manipulated attractiveness of males. This demonstrates that, in this socially monogamous species of bird, attractiveness of males could be considered to be a social construct, at least partially determined via social feedback from females.     

Occurrence of extra-pair copulation in the tree swallow (Tachycineta bicolor)

Summary A new method to mark sperm transfer events between birds, using microspheres inserted into males' cloacae, was employed to assess the frequency of extra-pair copulation (EPC) in a population of tree swallows (Tachycineta bicolor) in Ontario, Canada, during the summer of 1988. We inserted 25 males with microspheres; spheres from 8 (32%) of these males were found in extra-pair females, from which we infer that males pursue a mixed reproductive strategy of monogamy coupled with seeking EPCs. The cloacae of 10 of 41 (24.4%) females were found to contain microspheres from non-mates. EPCs occur more frequently between neighboring birds than between non-neighbors. Only two within-pair copulations were detected with this method, suggesting that it underestimates the occurrence of all copulations, extra-pair or within-pair. Copulation watches revealed that within-pair copulations occur very frequently. We propose that frequent pair copulations are used by males to ensure their paternity in their mate's offspring. Offprint requests to: R.J. Robertson     

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     

Interactive effects of male and female age on extra-pair paternity in a socially monogamous seabird

Females sometimes obtain older sires for their offspring through extra-pair interactions, but how female age influences paternity is largely unexplored and interactive effects across the age span of both sexes have not been analyzed. To test whether female choice of sire age varies with female age in the blue-footed booby (Sula nebouxii), we examined associations between ages of both partners and the probability of extra-pair paternity (EPP) in 350 broods of parents up to 22 years old in a single breeding season. Extra-pair paternity enables a female to select an alternative sire for her offspring and could function to avoid or achieve particular combinations of parental ages. A male age?×?female age interaction revealed that in young females (≤4 years), EPP decreased with increasing age of the social partner, whereas in old females (≥8 years), it increased. Moreover, sires of extra-pair (EP) chicks of young females paired to young males were on average 6.33 years older than the females’ social partners. Since female boobies control copulatory access, this pattern could imply that young females choose old sires for their proven genetic quality and that old females avoid very old males because matings with them may risk infertility or genetic defects in offspring. Taking female age into account and observing across the whole age span may be necessary for understanding female age-based mate choice.     

Social experience during adolescence influences how male zebra finches (Taeniopygia guttata) group with conspecifics

Group-living animals rely on social skills which ensure beneficial interaction and prevent harmful ones with conspecifics. In a previous experiment, we demonstrated that male zebra finches reared in groups during adolescence show consistently less courtship and aggressive behaviour as adults than pair-reared males. Here we tested whether such differences affect how they group with conspecifics, as an indicator of their social integration. Zebra finches were kept in pairs (male–female or male–male) or mixed-sex groups (three males and three females) during adolescence and were introduced to an established group of unknown conspecifics during adulthood. Male courtship and aggressive behaviour were quantified directly after introduction to the group and 48 h later. At the same time, male position in relation to other birds and the number of birds in proximity were recorded. Males that grew up in a small mixed-sex group during adolescence spent more time within groups, were observed in bigger groups and lost less weight than males raised in pairs, indicating that an enriched social environment during early development may facilitate social integration. However, we observed no differences in courtship and aggressive behaviour that could predict the differences in grouping behaviour of pair- and group-reared males. We discuss alternative explanations for the difference in grouping and how to test these in future research.     

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.     

Parentally biased favouritism in relation to offspring sex in zebra finches

Family conflicts over parental care result in offspring attempting to exert control using solicitation behaviours, whilst the parents are potentially able to retaliate through provisioning rules. However, the evolutionary interests of one parent may not necessarily support the evolutionary interests of the other parent, and such conflicts of interest may be expressed in how the two parents allocate the same form of parental care to individual offspring. Theory suggests that such parentally biased favouritism is a universally predicted outcome of evolutionary conflicts of interest, and empirical evidence suggests that parentally biased favouritism occurs in relation to offspring size and solicitation behaviours. However, unequivocal empirical evidence of parentally biased favouritism in relation to offspring sex is absent, due to being strongly confounded by sex differences in size and solicitation behaviours. Here, we present strong evidence for parentally biased favouritism in relation to offspring sex in zebra finches (Taeniopygia guttata), independent of the effects of chick size and begging intensity. Mothers preferentially provisioned sons over daughters, whilst fathers showed no bias, meaning that sons received more food than daughters. Parentally biased favouritism in relation to offspring sex facilitates parental control over evolutionary conflicts of interest and is probably more widespread than previously realised.     

Individual differences in sampling behaviour predict social information use in zebra finches

When animals have to decide where to forage, what to eat or with whom to mate, they can base their decisions on either socially or personally acquired information. In accordance with theoretical predictions, there is experimental evidence that animals adjust the weight they give to both sources of information depending on circumstances. Notably, several studies have demonstrated that individuals rely more on social information when personal information is difficult to acquire or unreliable, because these conditions leave them uncertain as how to behave. Yet, even when individuals are exposed to the same conditions, they generally differ widely in the value they attribute to social and personal information. These differences suggest that the tendency to rely on social information would also depend on intrinsic characteristics that affect, for instance, individual efficiency in collecting personal information. To address this issue, we conducted laboratory experiments using female zebra finches (Taeniopygia guttata) and we tested them under three consecutive conditions. First, we evaluated their reliance on social information in a mating context and in a foraging context. Then, we measured their efficiency in acquiring personal information by recording their sampling behaviour when searching for hidden food. We found that females that sampled their environment less actively consistently relied on social information to a greater extent compared with those that invested more in sampling. Contrary to what is generally assumed, then, our study demonstrates that social information use is not entirely flexible and context dependent.     

Polygyny and extra-pair paternity enhance the opportunity for sexual selection in blue tits

Polygyny and extra-pair paternity are generally thought to enhance sexual selection. However, the extent to which these phenomena increase variance in male reproductive success will depend on the covariance between success at these two strategies. We analysed these patterns over four breeding seasons in facultatively polygynous blue tits Cyanistes caeruleus. We found that both polygyny and extra-pair paternity increased variance in male reproductive success and that standardised variance in annual number of genetic fledglings was 2.6 times higher than standardised variance in apparent success when assuming strict monogamy. Nevertheless, male success at securing within-pair paternity was unrelated to success at gaining extra-pair paternity and, when considering the positive effect of age on extra-pair success and attracting a second female, polygynous males were no more likely to sire extra-pair fledglings. Overall, polygynous males fledged more genetic offspring than monogamous males, but first-year polygynous males lost a greater share of within-pair paternity. A literature review suggests that this adverse effect of polygyny on within-pair paternity is frequent among birds, inconsistent with the prediction that females engage in extra-pair copulation with successful males to obtain good genes. Furthermore, a male's share of paternity was repeatable between years, and among females of polygynous males within years, such that a compatibility function of extra-pair copulations was likewise unsupported. Instead, we suggest that the observed patterns are most consistent with a fertility insurance role for extra-pair copulations, which does not exclude the greater opportunity for sexual selection through differential ability of males to gain paternity.     

Costing reproduction: effects of mating opportunity on mating success in male Bicyclus anynana butterflies

It is frequently assumed that males have an almost unlimited reproductive capacity, while access to receptive females is typically limiting. Consequently, sexual selection is expected to favor vigorous courtship behavior in males. If such behavior is associated with non-trivial costs, ample current mating opportunities should be accompanied by a reduction in future mating vigor. To test this hypothesis, three treatments differing in sex ratio were established using the tropical butterfly Bicyclus anynana: 50 males each were housed either with 0, 25, or 50 females. Mating trials involving the competition among males from each treatment for a single virgin female were carried out on days 3, 9, and 15 after allocation to treatments. While there was no difference on day 3, prior mating opportunity clearly reduced mating success on days 9 and 15, being lowest if identical numbers of males and females were housed together. This finding suggests accumulating costs associated with high courtship and/or mating activity. Further, older males were more active and initiated copulation earlier than the younger ones, consistent with the residual reproductive value hypothesis. We found no evidence for a survival or fertility cost of mating.     

Responses of male white ibises to their mate's extra-pair copulations

Summary I intensively observed the mating behavior of 134 pairs of white ibises for over 15 000 pair hours to examine the responses of males to extrapair copulations (EPC) involving their mates. Females often cooperated completely in apparently fertile EPCs. Male mate-guarding was vigorous and effective. Males did not respond to apparent sperm competition with forced-pair copulation, physical punishment, or abandonment of their mates. I found no negative correlation between degree of female promiscuity and the amount of parental care her mate gave to the entire brood. Males also did not reduce paternal care given to the young most likely to be the result of an EPC. I hypothesize that males are constrained in the behaviors they can use to avoid misplaced paternity in this species. While male mate-guarding reduces the opportunities for female involvement in EPC, the behaviors used by males to protect paternity apparently have not prevented the evolution of female receptiveness during EPC attempts.     

Singing activity stimulates partner reproductive investment rather than increasing paternity success in zebra finches

Song is used as a signal in sexual selection in a wide range of taxa. In birds, males of many species continue to sing after pair formation. It has been suggested that a high song output after pair formation might serve to attract extra-pair females and to minimise their own partner’s interest in extra-pair copulations. A non-exclusive alternative function that has received only scant attention is that the amount of song might stimulate the own female’s investment into eggs in a quantitative way. We address these hypotheses in a captive population of zebra finches, Taeniopygia guttata, by relating male undirected song output (i.e. non-courtship song) to male egg siring success and female reproductive investment in two different set-ups. When allowed to breed in aviaries, males with the highest song output were no more attractive than others to females in an analysis of 4,294 extra-pair courtships involving 164 different males, and they also did not sire more offspring (both trends were against the expectation). When breeding in cages with two different partners subsequently, females produced larger eggs with more orange yolks when paired to a male with a high song output. These findings suggest that singing activity in paired zebra finch males might primarily function to stimulate the partner and not to attract extra-pair females.     

Pair and extra-pair mating success relative to male quality in red-winged blackbirds

We tested whether the reproductive success of male red-winged blackbirds (Agelaius phoeniceus) varied with male secondary sexual traits or with haematozoa prevalence, and whether these patterns were consistent with females preferring genetically superior males. We also determined whether the traits that correlated with male success on their own territories were also correlated with male success at siring young on other males territories. Our analysis included data from a 6-year study involving 617 nestlings for which paternity was determined by DNA profiling. Larger males sired more young on their territories, principally because they obtained larger harems. The success of larger males at acquiring more mates did not appear to be a consequence of larger males holding larger or better-quality territories. Older and longer-lived males sired more young by extra-pair fertilizations. Larger males sired the most offspring overall (on territory + off territory). Variation in epaulet size and color, responses to male and female models, nest defence and parasitism was not correlated with male success either on or off their territories or overall. Male success in a given year was significantly correlated with success the previous year, as expected if females were selecting genetically superior males. The male that was by far the most successful individual in this study was highly consistent from year to year. Because male body size is positively correlated with survival in this population (although not within the sample of males included in this study), female preference for larger males may have reflected a general preference for males with superior Survival ability. We propose that the direct advantage realized by older males in extra-pair matings might indicate that experience is important, such that experienced males are better at creating or exploiting the opportunities for extra-pair mating. This hypothesis is consistent with a pairwise analysis of cuckoldry that showed that cuckolders were most often older than the males they cuckolded.     

Developmental stress affects song learning but not song complexity and vocal amplitude in zebra finches

Several recent studies have tested the hypothesis that song quality in adult birds may reflect early developmental conditions, specifically nutritional stress during the nestling period. Whilst all of these earlier studies found apparent links between early nutritional stress and song quality, their results disagree as to which aspects of song learning or production were affected. In this study, we attempted to reconcile these apparently inconsistent results. Our study also provides the first assessment of song amplitude in relation to early developmental stress and as a potential cue to male quality. We used an experimental manipulation in which the seeds on which the birds were reared were mixed with husks, making them more difficult for the parents to obtain. Compared with controls, such chicks were lighter at fledging; they were thereafter placed on a normal diet and had caught up by 100 days. We show that nutritional stress during the first 30 days of life reduced the birds’ accuracy of song syntax learning, resulting in poorer copies of tutor songs. Our experimental manipulations did not lead to significant changes in song amplitude, song duration or repertoire size. Thus, individual differences observed in song performance features probably reflect differences in current condition or motivation rather than past condition.     

Age-related changes in reproductive effort of male bison

Summary The behavior of male bison during the rut was studied, to test the prediction that reproductive effort should increase with age. Because bull bison do not show parental care, the major component of reproductive effort is competition with other bulls to obtain copulations with estrous females. Data were collected on activity budgets during the pre-rut and rut seasons, on interactions with other bulls, and on proximity to tended females during the rut. Participation in the rut started at ages 5–6. Older bulls showed greater percent time active and less percent time eating than younger bulls. The older bulls also had higher counts of dominance and fight-related interactions and lower counts for behavior associated with submission than did the younger bulls. Risk taken seemed to increase with age since bulls aged 6 to 12 participated more frequently in dangerous activities associated with fighting. Within the 6 to 12 year old group, activity patterns changed little with age. However, from the interaction information, peak ages of 8 to 11 years appeared. For the activities: back up, chase, clash, head nod, jump away, move away, run away, run toward, push heads, dominant, and risk, 11 and 12 year olds more closely resembled younger bulls. This suggests a reproductive effort curve that is flat at zero until about age 6, increases to age 8, flattens out again to around age 10, and then decreases somewhat. Reproductive effort in male bison thus generally conforms with life-history theory predictions.     

Strategic male signalling effort in a desert-dwelling fish

Males often use elaborate courtship displays to attract females for mating. Much attention, in this regard, has been focused on trying to understand the causes and consequences of signal variation among males. Far less, by contrast, is known about within-individual variation in signal expression and, in particular, the extent to which males may be able to strategically adjust their signalling output to try to maximise their reproductive returns. Here, we experimentally investigated male courtship effort in a fish, the Australian desert goby, Chlamydogobius eremius. When offered a simultaneous choice between a large and a small female, male gobies spent significantly more time associating with, and courting, the former, probably because larger females are also more fecund. Male signalling patterns were also investigated under a sequential choice scenario, with females presented one at a time. When first offered a female, male courtship was not affected by female size. However, males adjusted their courtship effort towards a second female depending on the size of the female encountered previously. In particular, males that were first offered a large female significantly reduced their courtship effort when presented with a subsequent, smaller, female. Our findings suggest that males may be able to respond adaptively to differences in female quality, and strategically adjust their signalling effort accordingly.