Barbara A. Caspers

Olfactory kin recognition in a songbird

The ability to recognize close relatives in order to cooperate or to avoid inbreeding is widespread across all taxa. One accepted mechanism for kin recognition in birds is associative learning of visual or acoustic cues. However, how could individuals ever learn to recognize unfamiliar kin? Here, we provide the first evidence for a novel mechanism of kin recognition in birds. Zebra finch (Taeniopygia guttata) fledglings are able to distinguish between kin and non-kin based on olfactory cues alone. Since olfactory cues are likely to be genetically based, this finding establishes a neglected mechanism of kin recognition in birds, particularly in songbirds, with potentially far-reaching consequences for both kin selection and inbreeding avoidance.

Odour-based natal nest recognition in the zebra finch (Taeniopygia guttata), a colony-breeding songbird

Passerine birds have an extensive repertoire of olfactory receptor genes. However, the circumstances in which passerine birds use olfactory signals are poorly understood. The aim of this study is to investigate whether olfactory cues play a role in natal nest recognition in fledged juvenile passerines. The natal nest provides fledglings with a safe place for sleeping and parental food provisioning. There is a particular demand in colony-breeding birds for fledglings to be able to identify their nests because many pairs breed close to each other. Olfactory orientation might thus be of special importance for the fledglings, because they do not have a visual representation of the nest site and its position in the colony when leaving the nest for the first time. We investigated the role of olfaction in nest recognition in zebra finches, which breed in dense colonies of up to 50 pairs. We performed odour preference tests, in which we offered zebra finch fledglings their own natal nest odour versus foreign nest odour. Zebra finch fledglings significantly preferred their own natal nest odour, indicating that fledglings of a colony breeding songbird may use olfactory cues for nest recognition.

SONGS, SCENTS, AND SENSES: SEXUAL SELECTION IN THE GREATER SAC-WINGED BAT, SACCOPTERYX BILINEATA

Abstract Like many other mammals, Saccopteryx bilineata exhibits a polygynous mating system, in which each male defends a group of females called a harem. Colonies consist of several harems, and nonharem males roost adjacent to harems. Unlike most other mammals, females disperse from their natal colony and most juvenile males remain in it. Thus, colonies consist of patrilines, which promotes intense local mate competition. Females are in estrus during a few weeks at the end of the rainy season. Mating is most likely initiated by females and preceded by intense courtship displays of males. Forty percent of colony males do not sire any offspring during their tenure in the colony, whereas a few males can sire up to 6 offspring in a single year. Males use olfactory, visual, and acoustic signals for courtship, and they demonstrate territory ownership by scent marks, low-frequency calls, and visual displays. Harem males sire on average more offspring than do nonharem males but produce only 30% of the offspring within their own harem territory, with 70% being sired by other harem males or nonharem males. Reproductive success of males increases with decreasing size, fluctuating asymmetry, and fundamental frequency of territorial calls. In addition, females that are closely related to the harem holder are more likely to mate with other males than with the harem holder. Sexual selection in S. bilineata is most likely influenced by intense local mate competition caused by scarce roosts and the patrilineal organization of colonies.

Sexual imprinting on a novel blue ornament in zebra finches

Sexual imprinting plays an important role for the development of mate preferences in birds. We tested whether male and female zebra finches Taeniopygia guttata sexually imprinted on an evolutionary novel trait, a blue feather on the forehead in parents. Additionally, we tested whether males and females would transfer a learned preference for the blue feather to a preference for blue leg bands, and whether a potential mate with two novel blue traits can amplify its attractiveness. Offspring were raised by parents in four different imprinting groups: (1) both parents unadorned; (2) the mother adorned only; (3) the father adorned only; (4) both parents adorned with the blue feather. After young reached maturity, we tested their mate preference for adorned and unadorned conspecifics of the opposite sex in binary choice tests. Females of the father adorned imprinting group sexually imprinted on the blue feather, and females reared by adorned parents showed a tendency to prefer adorned males. None of the males sexually imprinted on the blue feather. Our study replicates the results of a previous study on sexual imprinting on a red feather in zebra finches. We, therefore, propose a sex difference in the learning process of sexual imprinting. Females sexually imprinted on the blue feather did not transfer the learned preference to males with blue leg bands, and two novel blue traits could not amplify the attractiveness in males and females for the opposite sex. Our study emphasizes the role of sexual imprinting for the cultural evolution in mate preferences in zebra finches.

The more the better – polyandry and genetic similarity are positively linked to reproductive success in a natural population of terrestrial salamanders (Salamandra salamandra)

Although classically thought to be rare, female polyandry is widespread and may entail significant fitness benefits. If females store sperm over extended periods of time, the consequences of polyandry will depend on the pattern of sperm storage, and some of the potential benefits of polyandry can only be realized if sperm from different males is mixed. Our study aimed to determine patterns and consequences of polyandry in an amphibian species, the fire salamander, under fully natural conditions. Fire salamanders are ideal study objects, because mating, fertilization and larval deposition are temporally decoupled, females store sperm for several months, and larvae are deposited in the order of fertilization. Based on 18 microsatellite loci, we conducted paternity analysis of 24 female‐offspring arrays with, in total, over 600 larvae fertilized under complete natural conditions. More than one‐third of females were polyandrous and up to four males were found as sires. Our data clearly show that sperm from multiple males is mixed in the females spermatheca. Nevertheless, paternity is biased, and the most successful male sires on average 70% of the larvae, suggesting a ‘topping off’ mechanism with first‐male precedence. Female reproductive success increased with the number of sires, most probably because multiple mating ensured high fertilization success. In contrast, offspring number was unaffected by female condition and genetic characteristics, but surprisingly, it increased with the degree of genetic relatedness between females and their sires. Sires of polyandrous females tended to be genetically similar to each other, indicating a role for active female choice.

Bats, Bacteria, and Bat Smell: Sex-Specific Diversity of Microbes in a Sexually Selected Scent Organ

Abstract Microbes interfere with the olfactory communication of animals by degrading chemical signals or by adding volatile metabolites. We report on the composition and diversity of the microflora in a sexually selected scent organ, the wing sacs of Saccopteryx bilineata, which are used by males for courting females. Wing sacs lack any glandular tissues. Instead, males clean and refill their wing sacs each day with genital and gular secretions. Females have only a nonfunctional rudiment of this organ. We isolated a total of 40 microbial species with only a moderate overlap in species composition between the sexes. The estimated microbial diversity was significantly lower in males than in females, with a minimum of 52.5 microbial species ± 5.0 SD in wing sac rudiments of females and 40.3 ± 4.2 SD in wing sacs of males (jackknife estimates). Males carried on average only 2 out of 40 possible microbial species in their wing sacs. Thus, individual scent profiles of males could originate from individual microflora. The daily routine of wing sac cleaning and refilling has possibly evolved to control microbial scent degradation, to support an individual microflora involved via volatile metabolites in mate choice, or both. Microbes may play a more prominent role in the evolution of morphological structures and behavioral adaptations than previously envisaged.

The biology of color

In living color Animals live in a colorful world, but we rarely stop to think about how this color is produced and perceived, or how it evolved. Cuthill et al. review how color is used for social signals between individual animals and how it affects interactions with parasites, predators, and the physical environment. New approaches are elucidating aspects of animal coloration, from the requirements for complex cognition and perception mechanisms to the evolutionary dynamics surrounding its development and diversification. Science, this issue p. eaan0221 BACKGROUND The interdisciplinary field of animal coloration is growing rapidly, spanning questions about the diverse ways that animals use pigments and structures to generate color, the underlying genetics and epigenetics, the perception of color, how color information is integrated with information from other senses, and general principles underlying color’s evolution and function. People working in the field appreciate linkages between these parallel lines of enquiry, but outsiders need the easily navigable roadmap that we provide here. ADVANCES In the past 20 years, the field of animal coloration research has been propelled forward by technological advances that include spectrophotometry, digital imaging, computational neuroscience, innovative laboratory and field studies, and large-scale comparative analyses, which are allowing new questions to be asked. For example, we can now pose questions about the evolution of camouflage based on what a prey’s main predator can see, and we can start to appreciate that gene changes underlying color production have occurred in parallel in unrelated species. Knowledge of the production, perception, and evolutionary function of coloration is poised to make contributions to areas as diverse as medicine, security, clothing, and the military, but we need to take stock before moving forward. OUTLOOK Here, a group of evolutionary biologists, behavioral ecologists, psychologists, optical physicists, visual physiologists, geneticists, and anthropologists review this diverse area of science, daunting to the outsider, and set out what we believe are the key questions for the future. These are how nanoscale structures are used to manipulate light; how dynamic changes in coloration occur on different time scales; the genetics of coloration (including key innovations and the extent of parallel changes in different lineages); alternative perceptions of color by different species (including wavelengths that we cannot see, such as ultraviolet); how color, pattern, and motion interact; and how color works together with other modalities, especially odor. From an adaptive standpoint, color can serve several functions, and the resulting patterns frequently represent a trade-off among different evolutionary drivers, some of which are nonvisual (e.g., photoprotection). These trade-offs can vary between individuals within the same population, and color can be altered strategically on different time scales to serve different purposes. Lastly, interspecific differences in coloration, sometimes even observable in the fossil record, give insights into trait evolution. The biology of color is a field that typifies modern research: curiosity-led, technology-driven, multilevel, interdisciplinary, and integrative. Spectacular changes to color and morphology in a cuttlefish. Color can conceal or reveal. The giant Australian cuttlefish (Sepia apama) alters the relative size of its pigment-bearing chromatophores and warps its muscular skin to switch between camouflage mode (top) and communication mode (bottom) in under a second. Photos:

Chemical fingerprints encode mother–offspring similarity, colony membership, relatedness, and genetic quality in fur seals

Significance Understanding olfactory communication in natural vertebrate populations requires knowledge of how genes and the environment influence highly complex individual chemical fingerprints. To understand how relevant information is chemically encoded and may feed into mother–offspring recognition, we therefore generated chemical and genetic data for Antarctic fur seal mother–pup pairs. We show that pups are chemically highly similar to their mothers, reflecting a combination of genetic and environmental influences. We also reveal associations between chemical fingerprints and both genetic quality and relatedness, the former correlating positively with substance diversity and the latter encoded mainly by a small subset of substances. Dissecting apart chemical fingerprints to reveal subsets of potential biological relevance has broad implications for understanding vertebrate chemical communication. Chemical communication underpins virtually all aspects of vertebrate social life, yet remains poorly understood because of its highly complex mechanistic basis. We therefore used chemical fingerprinting of skin swabs and genetic analysis to explore the chemical cues that may underlie mother–offspring recognition in colonially breeding Antarctic fur seals. By sampling mother–offspring pairs from two different colonies, using a variety of statistical approaches and genotyping a large panel of microsatellite loci, we show that colony membership, mother–offspring similarity, heterozygosity, and genetic relatedness are all chemically encoded. Moreover, chemical similarity between mothers and offspring reflects a combination of genetic and environmental influences, the former partly encoded by substances resembling known pheromones. Our findings reveal the diversity of information contained within chemical fingerprints and have implications for understanding mother–offspring communication, kin recognition, and mate choice.

Are olfactory cues involved in nest recognition in two social species of estrildid finches

Reliably recognizing their own nest provides parents with a necessary skill to invest time and resources efficiently in raising their offspring and thereby maximising their own reproductive success. Studies investigating nest recognition in adult birds have focused mainly on visual cues of the nest or the nest site and acoustic cues of the nestlings. To determine whether adult songbirds also use olfaction for nest recognition, we investigated the use of olfactory nest cues for two estrildid finch species, zebra finches (Taeniopygia guttata) and Bengalese finches (Lonchura striata var. domestica) during the nestling and fledgling phase of their offspring. We found similar behavioural responses to nest odours in both songbird species. Females preferred the odour of their own nest over a control and avoided the foreign conspecific nest scent over a control during the nestling phase of their offspring, but when given the own odour and the foreign conspecific odour simultaneously we did not find a preference for the own nest odour. Males of both species did not show any preferences at all. The behavioural reaction to any nest odour decreased after fledging of the offspring. Our results show that only females show a behavioural response to olfactory nest cues, indicating that the use of olfactory cues for nest recognition seems to be sex-specific and dependent on the developmental stage of the offspring. Although estrildid finches are known to use visual and acoustic cues for nest recognition, the similar behavioural pattern of both species indicates that at least females gain additional information by olfactory nest cues during the nestling phase of their offspring. Thus olfactory cues might be important in general, even in situations in which visual and acoustic cues are known to be sufficient.

Odour-based species recognition in two sympatric species of sac-winged bats (Saccopteryx bilineata, S. leptura): combining chemical analyses, behavioural observations and odour preference tests

Combining chemical analysis and odour preference tests, we asked whether two closely related sympatric species of sac-winged bats use odour for species recognition. Males of the two sister species Saccopteryx bilineata and Saccopteryx leptura have pouches containing an odoriferous liquid in their antebrachial wing membrane, which is used in S. bilineata during courtship displays. Although both species occasionally share the same daytime roosts and are morphologically similar, there is no evidence for interbreeding. We compared the production and composition of the wing sac odorant in male S. leptura and S. bilineata and performed odour preference tests with female S. bilineata. Similar to male S. bilineata, male S. leptura cleansed and refilled their wing sacs with secretions, but they spent more time each day in doing so than male S. bilineata. Chemical analysis by gas chromatography and mass spectrometry revealed that male Saccopteryx carried species-specific scents in their wing sacs. Binary choice tests confirmed that female S. bilineata preferred the wing sac scents of male S. bilineata to those of the sister species, suggesting that the species specificity of male wing sac scents maintain the pre-mating isolation barrier between these closely related species.