Joah R. Madden

ANIMAL VISUAL SYSTEMS AND THE EVOLUTION OF COLOR PATTERNS: SENSORY PROCESSING ILLUMINATES SIGNAL EVOLUTION

Abstract Animal color pattern phenotypes evolve rapidly. What influences their evolution? Because color patterns are used in communication, selection for signal efficacy, relative to the intended receivers visual system, may explain and predict the direction of evolution. We investigated this in bowerbirds, whose color patterns consist of plumage, bower structure, and ornaments and whose visual displays are presented under predictable visual conditions. We used data on avian vision, environmental conditions, color pattern properties, and an estimate of the bowerbird phylogeny to test hypotheses about evolutionary effects of visual processing. Different components of the color pattern evolve differently. Plumage sexual dimorphism increased and then decreased, while overall (plumage plus bower) visual contrast increased. The use of bowers allows relative crypsis of the bird but increased efficacy of the signal as a whole. Ornaments do not elaborate existing plumage features but instead are innovations (new color schemes) that increase signal efficacy. Isolation between species could be facilitated by plumage but not ornaments, because we observed character displacement only in plumage. Bowerbird color pattern evolution is at least partially predictable from the function of the visual system and from knowledge of different functions of different components of the color patterns. This provides clues to how more constrained visual signaling systems may evolve.

Hypothesis testing in animal social networks

Behavioural ecologists are increasingly using social network analysis to describe the social organisation of animal populations and to test hypotheses. However, the statistical analysis of network data presents a number of challenges. In particular the non-independent nature of the data violates the assumptions of many common statistical approaches. In our opinion there is currently confusion and uncertainty amongst behavioural ecologists concerning the potential pitfalls when hypotheses testing using social network data. Here we review what we consider to be key considerations associated with the analysis of animal social networks and provide a practical guide to the use of null models based on randomisation to control for structure and non-independence in the data.

Sex, bowers and brains

Inter– and intraspecific variations in the sizes of specific avian brain regions correspond to the complexity of the behaviour that they govern. However, no study has demonstrated a relationship between gross brain size and behavioural complexity, a hypothesis that has been proposed to explain the unusually large human brain. I show, using X–rays of museum specimens, that species of bowerbirds that build bowers have relatively larger brains than both related and ecologically similar but unrelated species that do not build bowers. Bower design varies across species from simple cleared courts to ornate, hut–like structures large enough to contain a small child. Furthermore, species building more complex bowers have relatively larger brains, both within each of the two different bower–building clades and across the family as a whole, controlling for phylogeny. Such gross differences in brain size are surprising and may reflect the range of cognitive processes necessary for successful bower building. The relationships are strongest for males, the bower–building sex, although there is a similar trend in females. Because the size and complexity of bower design is targeted by female choice, the observation that relative brain size is related to bower complexity suggests that sexual selection may drive gross brain enlargement.

Performance in cognitive and problem-solving tasks in male spotted bowerbirds does not correlate with mating success.

Individuals exhibiting a high level of cognitive ability may also exhibit more elaborate traits and so gain higher levels of mating success. This suggests that selection may act on cognitive performance through mate choice. Studies investigating this relationship have tended to focus on single cognitive tasks, or tasks that are closely related to existing natural behaviours, and individuals are frequently tested in captive conditions. This can introduce test artefacts and may tell us more about selection on specific display behaviours that we imagine being particularly cognitively complex, rather than a general cognitive ability. We tested free-living male spotted bowerbirds, Ptilonorhynchus maculatus, that exhibit elaborate sexual displays which appear to be cognitively demanding. We describe a method for testing individuals in the wild, without the need for constraint or captivity. We looked for evidence of a general cognitive ability in males by assaying their performance in a series of novel tasks reflecting their natural bower-building behaviour (bower maintenance) or capturing more abstract measures of cognitive ability (colour and shape discrimination, reversal learning, spatial memory and motor skills). We related performance in these tasks to their mating success. An individuals performance in one task was a relatively poor predictor of performance in any other task. However, an individuals performance across tasks could be summarized by a principal component which explained a level of total variance above which has previously been accepted as evidence of a general cognitive ability. We found no relationships between an individuals overall performance, or performance in any single task, and mating success. Our results highlight the need for further investigation of whether selection on cognition in bowerbirds is exerted through mate choice. We offer this as an example of how classic cognitive tasks can be transferred to the wild, thus overcoming some limitations of captive cognitive testing.

Bower decorations attract females but provoke other male spotted bowerbirds: bower owners resolve this trade-off

Elaborate secondary sexual traits offset the costs that they impose on their bearer by facilitating reproductive benefits, through increased success in intrasexual contests or increased attractiveness to choosy mates. Some traits enhance both strategies. Conversely, I show that spotted bowerbirds Chlamydera maculata may face a trade–off. The trait that best predicts their mating success, numbers of Solanum berries exhibited on a bower, also provokes increased intrasexual aggression in the form of bower destructions by neighbouring bower owners, which reduce the quality of the males bower. At natural berry numbers, levels of mating success in the population are skewed, but levels of destruction do not vary with berry number. When berry numbers are artificially exaggerated, increased levels of destructions occur, but mating success does not increase. When offered excess berries, either to add to the bower or artificially placed on the bower, bower owners preferred to use numbers of berries related to the number that they displayed naturally. This decision is made without direct experience of the attendant changes in destruction or mating success. This indicates that bower owners may assess their own social standing in relation to their neighbours and modulate their display accordingly.

Nestling responses to adult food and alarm calls. 1. Species-specific responses in two cowbird hosts

Begging by nestlings can prove costly, either through energy expenditure if food-bearing parents are not present, or through increased predation risk. Therefore, parents may provide cues to modulate begging. We investigated responses of 7-day old nestlings of eastern phoebes, Sayornis phoebe, and red-winged blackbirds, Agelaius phoeniceus, to various adult calls. Phoebes begged strongly to playback of conspecific food calls but not to other vocal stimuli, and only weakly to manual stimulation. They had no specific response to phoebe alarm calls. We suggest that phoebe alarms, which were given mainly when a partner was nearby, at both egg and chick stages, function primarily to warn mates. Red-winged blackbirds begged most readily to manual stimulation and ceased begging, and crouched, specifically to conspecific alarm calls. Therefore, in phoebes begging is ‘switched on’, and in red-winged blackbirds it is ‘switched off’, by parental calls. We suggest that for species like red-winged blackbirds, which nest on flexible substrates, nestlings readily beg to vibrational cues such as nest movement, so parent alarms are important to switch off begging at inappropriate times. For species like phoebes, which nest on rigid substrates, food calls induce begging in the absence of vibrational stimuli, and may replace the need for alarm calls to nestlings. The marked differences seen in these hosts of the brown-headed cowbird, Molothrus ater, raises the question of whether nestlings of this generalist brood parasite can eavesdrop on such diversity in host cues, a problem we address in our companion paper.

Preferences for coloured bower decorations can be explained in a nonsexual context

Abstract The sensory bias model of sexual selection suggests that elaborate male secondary sexual traits evolved to exploit biases in the females sensory system. Such biases may have evolved in a nonsexual context. Male bowerbirds build and decorate elaborate structures, bowers, which function as targets of female choice. The colour of decorations used on bowers appears to be important in determining a males mating success. We tested two predictions made by the sensory bias model, using cache presentation experiments of artificially coloured grapes made to captive bowerbirds of five species. We first searched for evidence of ancestral biases for certain colours that could explain current colour preferences across species. We found no single parsimonious explanation for ancestral patterns of colour preference across the family. We next tested whether female preference patterns could be explained in a nonsexual, foraging, context. For both of the species where sufficient data could be collected, female foraging preferences for grapes were significantly related to male preferences for grapes used as bower decorations. Our results suggest that choice of bower decoration colour may have evolved to exploit a bias in the females sensory system, originally shaped by selection on foraging practices. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.

A host-race difference in begging calls of nestling cuckoos Cuculus canorus develops through experience and increases host provisioning

The structure of common cuckoo nestling begging calls differs between the two host-races parasitizing reed warblers (reed warbler-cuckoos) and dunnocks (dunnock-cuckoos; longer syllable duration, lower peak and maximum frequency, narrower bandwidth). Cross-fostering experiments demonstrated that this difference is not genetically fixed but develops through experience. When newly hatched reed warbler-cuckoos were transferred to dunnock nests, they developed begging calls more like those of dunnock-cuckoos, whereas controls transferred to the nests of robins or left to be raised by reed warblers developed calls more typical of reed warbler-cuckoos. We tested the effectiveness of these different calls in stimulating host provisioning by placing in host nests a single blackbird or song thrush nestling (of similar size to a young cuckoo, but lacking its exuberant begging calls); when it begged we broadcast, from a small loudspeaker on the nest rim, recordings of either dunnock-cuckoo or reed warbler-cuckoo begging calls. Playback of dunnock-cuckoo begging calls induced higher levels of provisioning by dunnocks, whereas playback of reed warbler-cuckoo begging calls did so for both reed warblers and robins. We suggest that the young cuckoo (which ejects the hosts eggs/chicks and so is raised alone) learns by experience which calls best stimulate host provisioning.

Integrating contact network structure into tuberculosis epidemiology in meerkats in South Africa: Implications for control

Empirical studies that integrate information on host contact patterns with infectious disease transmission over time are rare. The aims of this study were to determine the relative importance of intra-group social interactions in the transmission of tuberculosis (TB; Mycobacterium bovis infection) in a population of wild meerkats (Suricata suricatta) in South Africa, and to use this information to propose an evidence-based intervention strategy to manage this disease. Detailed behavioural observations of all members of eight meerkat groups (n=134 individuals) were made over 24 months from January 2006 to December 2007. Social network analysis of three types of interaction (aggression, foraging competitions and grooming) revealed social structure to be very stable over time. Clustering of interactions was positively correlated with group size for both aggression (r=0.73) and grooming interactions (r=0.71), suggesting that infections may spread locally within clusters of interacting individuals but be limited from infecting all members of large groups by an apparent threshold in connections between different clusters. Repeated biological sampling every three months of all members of one social group (n=37 meerkats) was undertaken to quantify individual changes in M. bovis infection status. These empirical data were used to construct a dynamic network model of TB transmission within a meerkat group. The results indicated that grooming (both giving and receiving) was more likely than aggression to be correlated with M. bovis transmission and that groomers were at higher risk of infection than groomees. Intervention strategies for managing TB in meerkats that focus on those individuals engaging in the highest amount of grooming are therefore proposed.

A host-race of the cuckoo Cuculus canorus with nestlings attuned to the parental alarm calls of the host species

The common cuckoo has several host-specific races, each with a distinctive egg that tends to match its hosts eggs. Here, we show that the host-race specializing on reed warblers also has a host-specific nestling adaptation. In playback experiments, the nestling cuckoos responded specifically to the reed warblers distinctive ‘churr’ alarm (given when a predator is near the nest), by reducing begging calls (likely to betray their location) and by displaying their orange-red gape (a preparation for defence). When reed warbler-cuckoos were cross-fostered and raised by two other regular cuckoo hosts (robins or dunnocks), they did not respond to the different alarms of these new foster-parents. Instead, they retained a specific response to reed warbler alarms but, remarkably, increased both calling and gaping. This suggests innate pre-tuning to reed warbler alarms, but with exposure necessary for development of the normal silent gaping response. By contrast, cuckoo chicks of another host-race specializing on redstarts showed no response to either redstart or reed warbler alarms. If host-races are restricted to female cuckoo lineages, then chick-tuning in reed warbler-cuckoos must be under maternal control. Alternatively, some host-races might be cryptic species, not revealed by the neutral genetic markers studied so far.