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.     

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.     

Testosterone upregulates lipoprotein status to control sexual attractiveness in a colorful songbird

A salient feature of many secondary sexual characteristics in animals is that their expression is controlled by sex-steroid hormones. However, for only a few types of ornaments do we know the precise molecular mechanism by which androgens like testosterone (T) enhance trait production. We studied the red carotenoid-based beak of male zebra finches (Taeniopygia guttata), which serves as a sexually selected trait and is thought to be T dependent. In previous research, we demonstrated that the extent to which male finches produce lipoproteins in the bloodstream, which bind carotenoid pigments acquired from the diet and transport them to peripheral tissues, regulates the accumulation of carotenoids in the body and beak pigmentation. Here we show that T acts to upregulate lipoprotein production and allows male zebra finches to display flashy, sexually attractive coloration. Levels of circulating T in blood positively and significantly predicted lipoprotein profile (as measured by cholesterol levels), blood carotenoid concentration, and beak color. Exogenous T administration elevated cholesterol and carotenoid status as well as beak redness. Last, experimental inhibition of T (using the anti-androgen flutamide) downregulated lipoprotein production and carotenoid circulation and faded the beak. This androgen- and lipoprotein-mediated system represents one of the more detailed physiological mechanisms underlying the development of a sex-steroid-dependent trait in animals.     

Male bill colour and age are associated with parental abilities and breeding performance in blackbirds

In monogamous bird species, male parental investment may influence offspring fitness and females may gain advantages through mating with males providing extensive paternal care. However, paternal care is a benefit that can only be assessed indirectly because mate choice precedes paternal activities. Individual quality and age, both signalled by morphological characteristics, may reflect parental abilities. Because they may reflect individual foraging abilities, carotenoid-based colorations have been proposed to honestly signal parental quality. The blackbird (Turdus merula), a socially monogamous species, exhibits biparental care and males show bills that vary from pale yellow to orange due to carotenoid pigments. In this study, we investigated whether male bill colour and age are associated with parental ability. Our results suggest that males with more orange bills and older males are better fathers. Indeed, male visit rate increased with their bill colour index independently of age, and brood condition was higher for adult males, compared to yearlings, independently of bill colour. Overall, the number of fledglings produced was positively influenced by both the age of males and the colour intensity of their bills. Males with more orange bills and adults had a greater number of fledglings and these males also had higher levels of prolactin, a hormone known to promote parental care. This latter finding suggests that prolactin may be the link between carotenoid based colorations and the intensity of paternal effort. Thus, male bill colour seems to honestly reveal male physiological adjustment to paternal activities.     

Defensive secretion of a flightless grasshopper: Failure to prevent lizard attack

Summary We tested the role of a grasshopper defensive secretion in deterring lizard predation. Adults, but not young larvae, of the chemically defended lubber grasshopperRomalea guttata (=microptera) froth a volatile secretion when attacked by predators. The lizardAnolis carolinensis failed to strike juvenile lubbers (which lack secretion) in laboratory trials. Survivorship of palatable crickets loaded with secretion offered toA. carolinensis was not significantly different from survivorship of control crickets. In experiments designed to investigate if lizards learn an aversion to the secretion, striking times forSceloporus undulatus fed wax worms coated with secretion were not significantly different over three days of trials. Three primary conclusions are drawn from these data. First, the secretion may not be necessary for lubber protection from lizards. Second, lubber secretion does not appear to deter lizards from attacking or eating prey items. Third, lizards do not appear to develop an aversion to the secretion.     

Population differentiation in female sex pheromone and male preferences in a solitary bee

Population differentiation in female mating signals and associated male preferences can drive reproductive isolation among segregated populations. We tested this assumption by investigating intraspecific variation in female sex pheromone and associated male odour preferences among distant populations in the solitary bee Colletes cunicularius (L.) by using quantitative gas chromatography and by performing field bioassays with synthetic blends of key sex pheromone compounds. We found significant differences in sex pheromone blends among the bee populations, and the divergence in odour blends correlated positively with geographic distance, suggesting that genetic divergence among distant populations can affect sex pheromone chemistry. Our behavioural experiments, however, demonstrate that synthetic copies of allopatric female sex pheromones were cross-attractive to patrolling males from distant populations, making reproductive isolation by non-recognition of mating signals among populations unlikely. Our data also show that patrolling male bees from different populations preferred odour types from allopatric populations at the two sites of bioassays. These male preferences are not expected to select for changes in the female sex pheromone, but may influence the evolution of floral odour in sexually deceptive orchids of the genus Ophrys that are pollinated by C. cunicularius males.     

Mate choice in the yellow-shouldered widowbird: correlates of male attractiveness

Recent investigations of male ornaments in sexual selection have used experimental manipulation of tail length in three widowbird species, but only for one of these have correlates of male reproductive success been reported. I examined correlates of male attractiveness to nesting females over two breeding seasons for the polygynous yellow-shouldered widowbird, Euplectes macrourus, in order to discover which cues females may be using to select mates. The black, long-tailed ( 10 cm) males defend large territories and build nest frames, or cock's nests, which females then line and use for nesting. I examined various aspects of male morphology, five behavioral displays, territory characteristics, and the number of cock's nests that males built. Few correlates of mating success were found. The best predictor was the number of cock's nests that a male builds, though one courtship display also correlated with male mating success in 1 year, as did average grass height. Tail length did not correlate with male mating success. A partial correlation analysis confirmed that cock's nests and, in 1 year, grass height, were the primary contributers to male success. Females may choose where to nest primarily on the availability of suitable nesting sites. Long tails may be used by females seeking extra-pair copulations or in male-male competition for territories.     

Female reactions to male absence after pairing in the pied flycatcher

Mating with an already mated pied flycatcher (Ficedula hypoleuca) male is costly for a female. Two hypotheses explain why some females still mate with already mated males. The deception hypothesis suggests that some females mate with already mated males since it is difficult to assess perfectly the mating status of a male with separate territories (polyterritoriality). The search cost hypothesis states that females are aware of male mating status but the costs of searching for an unmated male exceed costs associated with the status of secondary female. One potential cue that could disclose a male's mating status is the existence of brief visits to the primary territory by polyterritorial males. To mimic such visits I removed the male from the territory for 60 min soon after female settlement. Only few females abandoned their mates as a consequence of male removal even though they had available unmated males close by. This result is most consistent with the deception hypothesis. Females did not use occasional male absence as a cue to avoid presumably polyterritorial males and in this respect they were not perfect in assessing males.     

High paternal investment in unrelated young: extra-pair paternity and male parental care in house martins

The response of males to reduced paternity has important consequences for the evolution and maintenance of a mixed reproductive strategy. Paternity is predicted to affect directly the level of male parental care in some cases but not in others. The response of males to reduced paternity will be influenced by their ability to assess their paternity, the predictability of cuckoldry and the costs and benefits of parental care. Although male house martins (Delichon urbica) provide among the highest levels of male parental care known in passerines (incubation, brooding and feeding nestlings), there was no evidence that cuckolded males substantially reduced their level of parental care, and, as a result, all young fledged successfully. Thus, extra-pair fertilizations enhanced the reproductive success of some males because they were able to parasitize the parental care of cuckolded males. We discuss several conditions which may favor extensive male parental care even when the male's paternity is very low.     

Determinants of male reproductive success in wild long-tailed macaques (Macaca fascicularis)—male monopolisation, female mate choice or post-copulatory mechanisms?

One of the basic principles of sexual selection is that male reproductive success should be skewed towards strong males in species with anisogamous sex. Studies on primate multi-male groups, however, suggest that other factors than male fighting ability might also affect male reproductive success. The proximate mechanisms leading to paternity in multi-male primate groups still remain largely unknown since in most primate studies mating rather than reproductive success is measured. Furthermore, little research focuses on a female’s fertile phase. The aim of this study was to investigate the relative importance of male monopolisation and female direct mate choice for paternity determination. We also investigated the extent to which paternity was decided post-copulatory, i.e. within the female reproductive tract. We used a combined approach of behavioural observations with faecal hormone and genetic analysis for assessment of female cycle stage and paternity, respectively. The study was carried out on a group of wild long-tailed macaques living around the Ketambe Research Station, Gunung Leuser National Park, Indonesia. Our results suggest that both male monopolisation and post-copulatory mechanisms are the main determinants of male reproductive success, whereas female direct mate choice and alternative male reproductive strategies appear to be of little importance in this respect. Female cooperation may, however, have facilitated male monopolisation. Since paternity was restricted to alpha and beta males even when females mated with several males during the fertile phase, it seems that not only male monopolisation but also post-copulatory mechanisms may operate in favour of high-ranking males in long-tailed macaques, thus reinforcing the reproductive skew in this species.     

Carotenoid-based colouration and ultraviolet reflectance of the sexual ornaments of grouse

Among the most familiar sexual signals are red, yellow, and orange sexual traits pigmented by carotenoids. Many birds can detect near-ultraviolet (UV) light, and UV signals can play key roles in mate choice. Grouse (Tetraonidae) exhibit bright carotenoid-dependent sexual ornaments, their supra-orbital combs, which to humans appear orange-red. Combs also reflect in the UV, which is not visible to humans but is likely to be visible to grouse. In male red grouse Lagopus lagopus scoticus, we show that comb UV reflectance decreases with increasing comb size and redness. By removing the epidermis of combs, where carotenoid pigments are, we show that the UV reflectance is a property of the dermis, underneath the red pigmented epidermis. Carotenoid pigmentation of combs acted as a mask to reduce reflectance by the dermis in the range 400–550 nm and in the UV, 300–400 nm. Patagium skin (non-ornamental skin under the wing) also reflects in the UV, but epidermis removal on this bare part tended to reduce UV reflectance, whereas removal of the red epidermis of combs increased UV reflectance. Males in better condition (greater body mass relative to size) had bigger and redder combs, but with less UV. Thus, carotenoid pigments of grouse combs are deposited on a white background with significant UV reflectance, which can influence how the signal is perceived by conspecifics. Carotenoid-based traits exhibit UV reflectance in a number of species, but how UV reflectance and carotenoid pigmentation influence colour remains little known for integumentary ornaments compared to plumage traits. UV vision is not uncommon in birds and other animals, so future studies should investigate how UV reflectance influences the perception of carotenoid-based signals of quality.     

Changes in singing behavior of male black-capped chickadees (Parus atricapillus) following mate removal

We removed the mates of ten male black-capped chickadees (Pares atricapillus) during the nest-building period to determine the effect of female presence on dawn singing. During the first dawn chorus following mate removal, males sang significantly longer, increased movement within their territory, and increased the percentage of their territory covered while singing. After the female was returned, these parameters returned to the pre-removal values. Males did not alter the frequency range or modal frequency of their songs when the mate was removed, nor did they change the degree of frequency shifting in the fee-bee song. We conclude that dawn singing in the black-capped chickadee acts, in part, as an intersexual signal, and that the behavior of frequency shifting in the song may be directed more toward rival males than females. Correspondence to: K. Otter     

How reliable are behavioral cues for assessment of male mating status in polyterritorial wood warblers,Phylloscopus sibilatrix?

It has been suggested that polyterritoriality in birds, i.e. mated males defending two spatially separated territories, deceives females into accepting polygyny against their best interest. Mated males singing on secondary territories should make it difficult for new arriving females to assess the mating status of unmated and mated males advertising to females. However, there have been objections to the deception hypothesis, suggesting that differences in territorial behavior between males of different mating status may make correct assessment possible. Polyterritorial males frequently leave their secondary territory to visit the female in the primary territory, thereby revealing their mating status to females in search of mates. The aim of this study is to investigate how reliable behavioral cues are in assessing the mating status of males in polyterritorial wood warblers. Our study shows that singing activity of mated males on secondary territories and unmated males was similar in the morning, while there was a significant difference in the afternoon. Unmated males spent, on average, more time on their territories than mated males spent on their secondary territories. However, there was considerable variation in both unmated and mated males in the frequency in which they left their territories. For instance, unmated males left their territories quite frequently early in the season compared to later. Hence, females must be able to interpret singing behavior and a male leaving his territory differently depending on time of the season and time of the day in order to correctly assess the mating status of advertising males. Estimating the increase in probability of finding an unmated male by using behavioral cues showed that females could increase the probability of finding an unmated male compared to random choice with respect to mating status. The uncertainty was, however, still considerable. The most important factor affecting the probability of finding an unmated male was the proportion of mated males on secondary territories compared to unmated males. Our study suggests that presence on a territory is not a reliable cue for the assessment of male mating status in polyterritorial wood warblers.     

Identification and biological activity of sex pheromone components from females of the plum moth Illiberis rotundata Jordan (Lepidoptera: Zygaenidae: Procridinae)

The plum moth, Illiberis rotundata Jordan (Lepidoptera: Zygaenidae: Procridinae), is a pest of orchards in Japan and China. Few chemical ecological studies have been directed towards the Zygaenidae and particularly the Procridinae. To investigate the sex pheromone of this species, extracts of pheromone glands from adult female I. rotundata were analyzed by coupled gas chromatography-electroantennography (GC-EAG) and coupled gas chromatography-mass spectrometry (GC-MS). Whilst GC-EAG on male moths showed an active peak, identified as 2-butyl (7Z)-dodecenoate, GC-MS also revealed the presence of the homologue 2-butyl (9Z)-tetradecenoate. Electroantennographic investigations, as well as field tests, strongly suggested the natural compounds to have the (R)-configuration at the stereogenic centre. Field results demonstrate 0.2 mg of a 1:1-mixture of (2R)-butyl (7Z)-dodecenoate and (2R)-butyl (9Z)-tetradecenoate to be a powerful lure that may be used in pest control measures against I. rotundata. The chemical structures of the new pheromone components show the same features as those of other zygaenid species: unsaturated fatty acids esterified with a short chain chiral alcohol. This is the first example of a two-component blend constituting the pheromone of a procridinid species.     

Experimentally elevated plasma levels of testosterone do not increase male reproductive success in blue tits

In temperate passerines, increased testosterone (T) levels during breeding mediate male aggressive and mating behaviour. If individual variability in T levels is reflected in behavioural differences during mating, males with higher T might gain higher reproductive success. This can be tested experimentally by elevating T levels. However, high exogenous T levels are known to have negative effects on male sperm production. This may reduce male fitness, particularly if sperm competition is intense. We experimentally elevated T levels in breeding blue tit males to investigate how T levels above the natural mean influence male reproductive success. Contrary to most—if not all—previous experimental manipulations of T levels in birds, we restricted the treatment with exogenous T to the time when females were fertile and T levels were naturally high in males. In blue tits, extra-pair paternity is an important component of male reproductive success, and its frequency is likely influenced by androgen-mediated behaviours such as mate attraction and aggression towards other males. Here we show that T-males were equally likely to become cuckolded and did not gain more extra-pair paternity than control males. Cuckolded T-males, however, lost more paternity than control males. We discuss the possibility that this is caused by negative effects of T treatment on sperm production.Communicated by M. Webster     

Dynamics of space use and male vigour amongst wood mice,Apodemus sylvaticus,in the cereal ecosystem

The spatial organisation of male and female wood mice,Apodemus sylvaticus, was investigated in a large-scale radio-tracking study on arable farmland near Oxford, United Kingdom, during the breeding season. Both sexes had significantly larger home ranges in the breeding season than at other times, and the breeding season home ranges of male (X = 1.44 ha) were significantly larger than those of females (X = 0.49 ha). Home range overlap was significantly greater between males, and between males and females, than it was between females. Overlap between males tended to be greatest in heavily utilised areas. Except during sexual consortship, there was minimal evidence of dynamic interaction among individuals. Home range sizes of breeding males varied widely, as did their body weights. There was no relationship between male body weight and home range size or any other movement parameter. However, males with the largest home ranges had the highest scores on all other movement parameters, indicating that they expended more energy in movement. These more vigorous males had access to the home ranges of more females than did males with small home ranges.     

Eggs of cabbage root fly stimulate conspecific oviposition: Evaluation of the activity and determination of an egg-associated compound

Summary. Previous studies indicated the presence of antennally-active compounds in extracts of eggs laid by female cabbage root flies, Delia radicum, that stimulated oviposition by conspecific females. We confirmed that previously laid D. radicum eggs stimulated oviposition by other D. radicum females, in a dose-dependent manner. Methanol extracts of conspecific eggs stimulated oviposition by females D. radicum, whereas egg extracts of D. antiqua and Psila rosae had no effect. Electrophysiological recordings from the tarsal sensilla of D. radicum females indicated that neurones of the C₅ sensillum responded to the egg extracts from both D. radicum and D. antiqua, but not P. rosae. Chemical analysis revealed that the extract of eggs from D. radicum contained the thia-triaza-fluorene compound, 1,2-dihydro-3-thia-4,10,10b-triaza-cyclopenta[.a.]fluorene-1-carboxylic acid (CIF-1), an oviposition stimulant found previously only in cruciferous plants. Another potentially active component has yet to be identified.     

Resource-holding power asymmetries,the prior residence effect,and reproductive payoffs in male northern elephant seal fights

The effect of resource-holding power (RHP) and prior residency asymmetries on fight outcome and subsequent seasonal copulatory success was analyzed for fights between marked male northern elephant seals (Mirounga angustirostris). RHP asymmetries were measured as differences in estimated mass and prior residency asymmetries were measured as differences in beach tenure prior to the fight. The principal results were: (a) Neither differences in mass nor differences in beach tenure had any effect on fight outcome as separate factors. (b) Mass and tenure differences had an interactive effect on fight outcome; fight winners were either heavier males present for shorter periods (intruders) or lighter males present for longer periods (prior residents). (c) Winners of fights copulated more often than losers after a fight throughout the breeding season; this difference was smallest for low-ranking males, larger for high-ranking males in short fights, and greatest for high-ranking males in long fights. (d) Prior resident males who won long fights obtained significantly more copulations after a fight than the males they defeated, but this was not true for intruder males who won long fights. These results suggest that male northern elephant seals will incur greater contest costs (i.e., fight for longer periods and/or against heavier males) for higher reproductive payoffs. They also imply that, at least for males in long fights, differences in prior residence represent payoff asymmetries, with higher reproductive payoffs for winning prior residents than for winning intruders.     

Preference for male traits in female wolf spiders varies with the choice of available males,female age and reproductive state

Individual variation in female preference for male traits may influence mate choice, especially if benefits and costs of choosiness vary with the range of available males or reproductive timing. We examined variation in female preference for male leg tuft size in Schizocosa ocreata (Hentz) wolf spiders with video playback. Dichotomous (simultaneous) choice test experiments included all possible combinations of four stimuli (i.e., modified versions of the same video male stimulus): average tuft size (control), reduced (−25%), enlarged (+25%), and no tufts (removed). Females exhibited a directional preference for larger tuft size independent of the nature of the choice (except for reduced tufts vs no tufts where no difference was seen). Female preference in the short term (over a period of 4 days) was also highly repeatable for control vs reduced tufts, but not for control vs enlarged tufts. Responses of females in ‘no-choice’ presentations of a single (control) male stimulus varied with age post-maturity; females were less receptive in weeks 1 and 2, highly receptive at week 3, and less thereafter. Mated females were least receptive and most aggressive towards a male stimulus. Females offered choices repeatedly at different ages post-maturity consistently preferred the control male vs reduced tufts over all 3 weeks but varied in their preference for enlarged tufts vs control male. In the first 2 weeks, females preferred the enlarged tuft male stimulus, but showed no preference by the third week. Females tested in week 4 showed no preference in either choice. Results suggest that the potential interaction between female preference for male traits and female reproductive timing may be a critical consideration in mate choice.     

Form-specific fragances fromOphrys insectifera L. (Orchidaceae) attract species of different pollinator genera. Evidence of sympatric speciation?

Two closely related forms ofOphrys insectifera were observed in the field to attract different pollinator species selectively.O. i. ssp.insectifera attracted males of two species ofArgogorytes (Sphecidae, Hymenoptera Aculeata) andO. i. ssp.aymoninii attractedAndrena combinata males (Andrenidae, Apoidea, Hymenoptera Aculeata). A third form,O. aff.i. ssp.insectifera, attracted none of these three species. Volatile compounds from flowers and inflorescences of the three forms (originating from Öland, Sweden, and Aveyron, France) were collected, using entrainment, enfleurage, and solvent extraction techniques, and identified by gas chromatography — mass spectrometry. Scent differences between the three forms were confirmed in the amounts of aliphatic hydrocarbons (C₁₁–C₁₉), methyl esters (C₁₄–C₁₈), short chain aliphatic 1-alcohols (C₆–C₁₂), and monoterpene alcohols (C₁₀).