Hanne Løvlie

Sophisticated sperm allocation in male fowl

When a female is sexually promiscuous, the ejaculates of different males compete for the fertilization of her eggs; the more sperm a male inseminates into a female, the more likely he is to fertilize her eggs. Because sperm production is limited and costly, theory predicts that males will strategically allocate sperm (1) according to female promiscuity, (2) saving some for copulations with new females, and (3) to females producing more and/or better offspring. Whether males allocate sperm in all of these ways is not known, particularly in birds where the collection of natural ejaculates only recently became possible. Here we demonstrate male sperm allocation of unprecedented sophistication in the fowl Gallus gallus. Males show status-dependent sperm investment in females according to the level of female promiscuity; they progressively reduce sperm investment in a particular female but, on encountering a new female, instantaneously increase their sperm investment; and they preferentially allocate sperm to females with large sexual ornaments signalling superior maternal investment. Our results indicate that female promiscuity leads to the evolution of sophisticated male sexual behaviour.

Sex-specific, counteracting responses to inbreeding in a bird

Inbreeding often depresses offspring fitness. Because females invest more than males in a reproductive event, inbreeding is expected to be more costly to mothers than fathers, creating a divergence between the reproductive interests of each sex and promoting sex–specific inbreeding strategies. Males and females may bias the probability of inbreeding by selecting copulation partners, and, in sexually promiscuous species, through male strategic sperm investment in different females and female selection of the sperm of different males. However, these processes are often difficult to study, and the way that different male and female strategies interact to determine inbreeding remains poorly understood. Here we demonstrate sex–specific, counteracting responses to inbreeding in the promiscuous red junglefowl, Gallus gallus. First, a male was just as likely to copulate with his full–sib sister as with an unrelated female. In addition, males displayed a tendency to: (i) initiate copulation faster when exposed to an unrelated female than when exposed to a sister, and (ii) inseminate more sperm into sisters than into unrelated females. Second, females retained fewer sperm following insemination by brothers, thus reducing the risk of inbreeding and counteracting male inbreeding strategies.

Cryptic preference for MHC-dissimilar females in male red junglefowl, Gallus gallus.

An increasing number of studies test the idea that females increase offspring fitness by biasing fertilization in favour of genetically compatible partners; however, few have investigated or controlled for corresponding preferences in males. Here, we experimentally test whether male red junglefowl, Gallus gallus, prefer genetically compatible females, measured by similarity at the major histocompatibility complex (MHC), a key gene complex in vertebrate immune function. Theory predicts that because some degree of MHC heterozygosity favours viability, individuals should prefer partners that carry MHC alleles different from their own. While male fowl showed no preference when simultaneously presented with an MHC-similar and an MHC-dissimilar female, they showed a ‘cryptic’ preference, by allocating more sperm to the most MHC-dissimilar of two sequentially presented females. These results provide the first experimental evidence that males might respond to the MHC similarity of a female through differential ejaculate expenditure. By revealing that cryptic male behaviours may bias fertilization success in favour of genetically compatible partners, this study demonstrates the need to experimentally disentangle male and female effects when studying preferences for genetically compatible partners.

Comparative support for the expensive tissue hypothesis: Big brains are correlated with smaller gut and greater parental investment in Lake Tanganyika cichlids

The brain is one of the most energetically expensive organs in the vertebrate body. Consequently, the energetic requirements of encephalization are suggested to impose considerable constraints on brain size evolution. Three main hypotheses concerning how energetic constraints might affect brain evolution predict covariation between brain investment and (1) investment into other costly tissues, (2) overall metabolic rate, and (3) reproductive investment. To date, these hypotheses have mainly been tested in homeothermic animals and the existing data are inconclusive. However, there are good reasons to believe that energetic limitations might play a role in large‐scale patterns of brain size evolution also in ectothermic vertebrates. Here, we test these hypotheses in a group of ectothermic vertebrates, the Lake Tanganyika cichlid fishes. After controlling for the effect of shared ancestry and confounding ecological variables, we find a negative association between brain size and gut size. Furthermore, we find that the evolution of a larger brain is accompanied by increased reproductive investment into egg size and parental care. Our results indicate that the energetic costs of encephalization may be an important general factor involved in the evolution of brain size also in ectothermic vertebrates.

Comparative support for the expensivetissue hypothesis: Big brains are correlatedwith smaller gut and greater parentalinvestment in Lake Tanganyika cichlids

The brain is one of the most energetically expensive organs in the vertebrate body. Consequently, the energetic requirements of encephalization are suggested to impose considerable constraints on brain size evolution. Three main hypotheses concerning how energetic constraints might affect brain evolution predict covariation between brain investment and (1) investment into other costly tissues, (2) overall metabolic rate, and (3) reproductive investment. To date, these hypotheses have mainly been tested in homeothermic animals and the existing data are inconclusive. However, there are good reasons to believe that energetic limitations might play a role in large‐scale patterns of brain size evolution also in ectothermic vertebrates. Here, we test these hypotheses in a group of ectothermic vertebrates, the Lake Tanganyika cichlid fishes. After controlling for the effect of shared ancestry and confounding ecological variables, we find a negative association between brain size and gut size. Furthermore, we find that the evolution of a larger brain is accompanied by increased reproductive investment into egg size and parental care. Our results indicate that the energetic costs of encephalization may be an important general factor involved in the evolution of brain size also in ectothermic vertebrates.

Male reproductive senescence causes potential for sexual conflict over mating.

The realization that senescence, age-dependent declines in survival and reproductive performance, pervades natural populations has brought its evolutionary significance into sharper focus. However, reproductive senescence remains poorly understood because it is difficult to separate male and female mechanisms underpinning reproductive success. We experimentally investigated male reproductive senescence in feral fowl, Gallus gallus domesticus, where socially dominant males monopolize access to females and the ejaculates of multiple males compete for fertilization. We detected the signal of senescence on multiple determinants of male reproductive success. The effect of age on status was dependent upon the intensity of intrasexual competition: old males were less likely to dominate male-biased groups where competition is intense but were as likely as young males to dominate female-biased groups. Mating and fertilization success declined sharply with male age largely as a result of population-level patterns. These age-dependent declines translated into sexually antagonistic payoffs: old males fertilized more eggs when they were dominant, but this resulted in females suffering a drastic reduction in fertility. Thus, male senescence causes potential for sexual conflict over mating, and the intensity of this conflict is modulated socially, by the probability of old males dominating reproductive opportunities.

Social status and personality: stability in social state can promote consistency of behavioural responses

Stability of ‘state’ has been suggested as an underlying factor explaining behavioural stability and animal personality (i.e. variation among, and consistency within individuals in behavioural responses), but the possibility that stable social relationships represent such states remains unexplored. Here, we investigated the influence of social status on the expression and consistency of behaviours by experimentally changing social status between repeated personality assays. We used male domestic fowl (Gallus gallus domesticus), a social species that forms relatively stable dominance hierarchies, and showed that behavioural responses were strongly affected by social status, but also by individual characteristics. The level of vigilance, activity and exploration changed with social status, whereas boldness appeared as a stable individual property, independent of status. Furthermore, variation in vocalization predicted future social status, indicating that individual behaviours can both be a predictor and a consequence of social status, depending on the aspect in focus. Our results illustrate that social states contribute to both variation and stability in behavioural responses, and should therefore be taken into account when investigating and interpreting variation in personality.

Sex-specific responses to sexual familiarity, and the role of olfaction in Drosophila.

Studies of mating preferences have largely neglected the potential effects of individuals encountering their previous mates (‘directly sexually familiar’), or new mates that share similarities to previous mates, e.g. from the same family and/or environment (‘phenotypically sexually familiar’). Here, we show that male and female Drosophila melanogaster respond to the direct and phenotypic sexual familiarity of potential mates in fundamentally different ways. We exposed a single focal male or female to two potential partners. In the first experiment, one potential partner was novel (not previously encountered) and one was directly familiar (their previous mate); in the second experiment, one potential partner was novel (unrelated, and from a different environment from the previous mate) and one was phenotypically familiar (from the same family and rearing environment as the previous mate). We found that males preferentially courted novel females over directly or phenotypically familiar females. By contrast, females displayed a weak preference for directly and phenotypically familiar males over novel males. Sex-specific responses to the familiarity of potential mates were significantly weaker or absent in Orco1 mutants, which lack a co-receptor essential for olfaction, indicating a role for olfactory cues in mate choice over novelty. Collectively, our results show that direct and phenotypic sexual familiarity is detected through olfactory cues and play an important role in sex-specific sexual behaviour.

Scent of the enemy: behavioural responses to predator faecal odour in the fowl

Chemical communication is used by diverse organisms in a variety of contexts and can have strong fitness consequences for the individuals involved. However, despite the extensive use of birds as models for many research areas in biology, avian olfaction has been poorly investigated. Studies on bird species that lack well-developed olfactory organs and those investigating responses to predator odours are particularly scarce. We investigated behavioural responses of the domestic fowl, Gallus gallus domesticus, a ground-living species with intermediate olfactory bulb size, to several predator and nonpredator faecal odours. We found that the birds spent less time foraging and were more vigilant when exposed to predator faecal odour compared with nonpredator faecal odour. Individuals showed a similar response when exposed to increased amounts of faeces. Taken together, our results demonstrate that domestic fowl can distinguish between herbivore and predator faecal odour, and respond to predator olfactory cues alone, without prior experience. Our results have implications for the understanding of predator–prey interactions and responses to olfactory cues in general, and for chemical communication in avian species more specifically.

Male mounting alone reduces female promiscuity in the fowl

The fertilization success of an insemination is at risk when a female has the possibility to copulate with multiple males, generating sperm competition and sexual conflict over remating. Female propensity to remate is often reduced after copulation, and a staggering diversity of highly derived male traits that discourage female promiscuity have been investigated. However, it is difficult to separate the effect of such specialized traits and insemination products from the more basic effect that the act of mounting per se may have on female remating. Here, we use a novel approach that separates the influence of mounting from that of insemination on female remating in the promiscuous feral fowl. Mounting alone caused a transient but drastic reduction in female propensity to remate, and-crucially-the number of sperm that a female obtained from a new male. Therefore, like other taxa, female fowl show a reduction in promiscuity after copulation, but this is entirely due to mounting alone. This effect of mounting, independent of insemination and fertilization, indicates that even copulations that deliver little or no semen, a puzzling behavior common in many species including the fowl, may play a crucial role in sperm competition.