An infrared motion detector system for lossless real-time monitoring of animal preference tests.

Automated behavioural observations are routinely used in many fields of biology, including ethology, behavioural ecology and physiology. When preferences for certain resources are investigated, the focus is often on simple response variables, such as duration and frequency of visits to choice chambers. Here we present an automated motion detector system that use passive infrared sensors to eliminate many drawbacks of currently existing methods. Signals from the sensors are processed by a custom-built interface, and after unnecessary data is filtered by a computer software, the total time and frequency of the subject's visits to each of the choice chambers are calculated. We validate the detector system by monitoring (using the system) and in the same time video recording mating preferences of zebra finches in a four-way choice apparatus. Manual scoring of the video recordings showed very high consistency with data from the detector system both for time and for frequency of visits. Furthermore, the validation revealed that if we used micro-switches or light barriers, the most commonly applied automatic detection techniques, this would have resulted in approximately 22% less information compared to our lossless system. The system provides a low-cost alternative for monitoring animal movements, and we discuss its further applicability.

Adult sex ratio variation: implications for breeding system evolution.

Adult sex ratio (ASR) exhibits immense variation in nature, although neither the causes nor the implications of this variation are fully understood. According to theory, the ASR is expected to influence sex roles and breeding systems, as the rarer sex in the population has more potential partners to mate with than the more common sex. Changes in mate choice, mating systems and parental care suggest that the ASR does influence breeding behaviour, although there is a need for more tests, especially experimental ones. In the context of breeding system evolution, the focus is currently on operational sex ratios (OSRs). We argue that the ASR plays a role of similar importance and urge researchers to study the ASR and the OSR side by side. Finally, we plead for a dynamic view of breeding system evolution with feedbacks between mating, parenting, OSR and ASR on both ecological and evolutionary time scales.

Why care? Inferring the evolution of complex social behaviour.

Phylogenetic comparative analyses of complex traits often reduce the traits of interests into a single (or a few) component variables. Here, we show that this may be an over-simplification, because components of a complex trait may evolve independently from each other. Using eight components of parental care in 400 bird species from 89 avian families that represent the relative contribution of male vs. female to a particular type of care, we show that some components evolve in a highly correlated manner, whereas others exhibit low (or no) phylogenetic correlation. Correlations were stronger within types of parental activity (brooding, feeding, guarding) than within stages of the breeding cycle (incubation, prefledging care, post-fledging care). A phylogenetically corrected cluster analysis identified two groups of parental care components that evolved in a correlated fashion: one group included incubation and brooding, whereas the other group comprised of the remaining components. The two groups of components provide working hypotheses for follow-up studies to test the underlying genetic, developmental and ecological co-evolutionary mechanism between male and female care. Furthermore, the components within each group are expected to respond consistently to different ambient and social environments.

Sexual selection on brain size in shorebirds (Charadriiformes).

Natural selection is considered a major force shaping brain size evolution in vertebrates, whereas the influence of sexual selection remains controversial. On one hand, sexual selection could promote brain enlargement by enhancing cognitive skills needed to compete for mates. On the other hand, sexual selection could favour brain size reduction due to trade-offs between investing in brain tissue and in sexually selected traits. These opposed predictions are mirrored in contradictory relationships between sexual selection proxies and brain size relative to body size. Here, we report a phylogenetic comparative analysis that highlights potential flaws in interpreting relative brain size-mating system associations as effects of sexual selection on brain size in shorebirds (Charadriiformes), a taxonomic group with an outstanding diversity in breeding systems. Considering many ecological effects, relative brain size was not significantly correlated with testis size. In polyandrous species, however, relative brain sizes of males and females were smaller than in monogamous species, and females had smaller brain size than males. Although these findings are consistent with sexual selection reducing brain size, they could also be due to females deserting parental care, which is a common feature of polyandrous species. Furthermore, our analyses suggested that body size evolved faster than brain size, and thus the evolution of body size may be confounding the effect of the mating system on relative brain size. The brain size-mating system association in shorebirds is thus not only due to sexual selection on brain size but rather, to body size evolution and other multiple simultaneous effects.

Persistence of an extreme male-biased adult sex ratio in a natural population of polyandrous bird.

In a number of insects, fishes and birds, the conventional sex roles are reversed: males are the main care provider, whereas females focus on matings. The reversal of typical sex roles is an evolutionary puzzle, because it challenges the foundations of sex roles, sexual selection and parental investment theory. Recent theoretical models predict that biased parental care may be a response to biased adult sex ratios (ASRs). However, estimating ASR is challenging in natural populations, because males and females often have different detectabilities. Here, we use demographic modelling with field data from 2101 individuals, including 579 molecularly sexed offspring, to provide evidence that ASR is strongly male biased in a polyandrous bird with male-biased care. The model predicts 6.1 times more adult males than females (ASR=0.860, proportion of males) in the Kentish plover Charadrius alexandrinus. The extreme male bias is consistent between years and concordant with experimental results showing strongly biased mating opportunity towards females. Based on these results, we conjecture that parental sex-role reversal may occur in populations that exhibit extreme male-biased ASR.

Domestic chickens defy Rensch's rule: sexual size dimorphism in chicken breeds.

Sexual size dimorphism (SSD), i.e. the difference in sizes of males and females, is a key evolutionary feature that is related to ecology, behaviour and life histories of organisms. Although the basic patterns of SSD are well documented for several major taxa, the processes generating SSD are poorly understood. Domesticated animals offer excellent opportunities for testing predictions of functional explanations of SSD theory because domestic stocks were often selected by humans for particular desirable traits. Here, we analyse SSD in 139 breeds of domestic chickens Gallus gallus domesticus and compare them to their wild relatives (pheasants, partridges and grouse; Phasianidae, 53 species). SSD was male-biased in all chicken breeds, because males were 21.5 ± 0.55% (mean ± SE) heavier than females. The extent of SSD did not differ among breed categories (cock fighting, ornamental and breeds selected for egg and meat production). SSD of chicken breeds was not different from wild pheasants and allies (23.5 ± 3.43%), although the wild ancestor of chickens, the red jungle fowl G. gallus, had more extreme SSD (male 68.8% heavier) than any domesticated breed. Male mass and female mass exhibited positive allometry among pheasants and allies, consistently with the Rensch's rule reported from various taxa. However, body mass scaled isometrically across chicken breeds. The latter results suggest that sex-specific selection on males vs. females is necessary to generate positive allometry, i.e. the Rensch's rule, in wild populations.

Evolution of sexual size dimorphism in grouse and allies (Aves: Phasianidae) in relation to mating competition, fecundity demands and resource division.

Sexual size dimorphism (SSD) is often assumed to be driven by three major selective processes: (1) sexual selection influencing male size and thus mating success, (2) fecundity selection acting on females and (3) inter-sexual resource division favouring different size in males and females to reduce competition for resources. Sexual selection should be particularly strong in species that exhibit lek polygyny, since male mating success is highly skewed in such species. We investigated whether these three selective processes are related to SSD evolution in grouse and allies (Phasianidae). Male-biased SSD increased with body size (Rensch's rule) and lekking species exhibited more male-biased SSD than nonlekking ones. Directional phylogenetic analyses indicated that lekking evolved before SSD, but conclusions were highly dependent on the body size traits and chosen model values. There was no relationship between SSD and male display agility, nor did resource division influence SSD. Although clutch mass increased with female body size it was not related to the degree of SSD. Taken together, the results are most consistent with the hypothesis that lekking behaviour led to the evolution of male-biased SSD in Phasianidae.

How is sexual conflict over parental care resolved? A meta-analysis.

Biparental care of offspring is both a form of cooperation and a source of conflict. Parents face a trade-off between current and future reproduction: caring less for the current brood allows individuals to maintain energy reserves and increase their chances of remating. How can selection maintain biparental care, given this temptation to defect? The answer lies in how parents respond to changes in each other's effort. Game-theoretical models predict that biparental care is evolutionarily stable when reduced care by one parent leads its partner to increase care, but not so much that it completely compensates for the lost input. Experiments designed to reveal responses to reduced partner effort have mainly focused on birds. We present a meta-analysis of 54 such studies, and conclude that the mean response was indeed partial compensation. Males and females responded differently and this was in part mediated by the type of manipulation used.

Are parental care trade-offs in shorebirds driven by parental investment or sexual selection?

Sexual selection, mating systems and parental behaviour are closely linked, although the exact nature of their relationship is controversial. The parental investment hypothesis (PIH) states that parental care disparity drives sexual selection intensity, because the sex providing less care competes for the sex that provides more. In contrast, the sexual selection hypothesis (SSH) asserts that more intense sexual selection on males leads to reduced male parental investment. We tested these hypotheses using directional phylogenetic comparative methods in shorebirds, which have an unusually diverse array of breeding systems. Changes in parental care and sexual selection intensity were tightly correlated, and we carried out three sets of analyses focusing on changes in male behaviour, female behaviour and in either sex. The results from the analyses were consistent with both PIH and SSH, although the patterns in male transition were sensitive to model values. We propose two explanations for these results. First, phylogenetic transitions may be idiosyncratic so that they depend on the ecological circumstances of individual species. Second, transitions in social traits, such as breeding systems, may be rapid and take place in ecological time, so directional phylogenetic methods that work through longer time scales may not infer accurately the timing and direction of all changes.

Sexual selection, sexual size dimorphism and Rensch's rule in Odonata.

Odonata (dragonflies and damselflies) exhibit a range of sexual size dimorphism (SSD) that includes species with male-biased (males > females) or female-biased SSD (males < females) and species exhibiting nonterritorial or territorial mating strategies. Here, we use phylogenetic comparative analyses to investigate the influence of sexual selection on SSD in both suborders: dragonflies (Anisoptera) and damselflies (Zygoptera). First, we show that damselflies have male-biased SSD, and exhibit an allometric relationship between body size and SSD, that is consistent with Rensch's rule. Second, SSD of dragonflies is not different from unit, and this suborder does not exhibit Rensch's rule. Third, we test the influence of sexual selection on SSD using proxy variables of territorial mating strategy and male agility. Using generalized least squares to account for phylogenetic relationships between species, we show that male-biased SSD increases with territoriality in damselflies, but not in dragonflies. Finally, we show that nonagile territorial odonates exhibit male-biased SSD, whereas male agility is not related to SSD in nonterritorial odonates. These results suggest that sexual selection acting on male sizes influences SSD in Odonata. Taken together, our results, along with avian studies (bustards and shorebirds), suggest that male agility influences SSD, although this influence is modulated by territorial mating strategy and thus the likely advantage of being large. Other evolutionary processes, such as fecundity selection and viability selection, however, need further investigation.

Parental conflict in birds: comparative analyses of offspring development, ecology and mating opportunities.

Parents often conflict over how much care to provide to their offspring. This conflict is expected to produce a negative relationship between male and female parental care, the strength of which may be mediated by both ecological and life-history variables. Previous studies have observed such trade-offs, but it is not known how generally they occur. Traditional views of sexual conflict place great importance on ecological factors in determining levels of parental care, whereas alternative views propose that the key determinant is mating opportunity. We carried out a broad-scale comparative study of parental conflict using 193 species from 41 families of birds. Using phylogenetic comparative analysis, we establish the generality of intersexual parental care conflict. We also show that parental conflict, as indicated by the disparity in care between the male and the female, depends on offspring development and mating opportunities, since in precocial species both males and females responded to increased mating opportunities. Altricial birds, however, failed to show these relationships. We also found little influence of breeding climate on parental conflict. Taken together, our results suggest that sexual conflict is a key element in the evolution of parental care systems. They also support the view that the major correlates of the intersexual conflict are mating opportunities for both sexes, rather than the breeding environment.

Sexual conflict over care: antagonistic effects of clutch desertion on reproductive success of male and female penduline tits.

A fundamental tenet of sexual conflict theory is that one sex may increase its reproductive success (RS) even if this harms the other sex. Several studies supported this principle by showing that males benefit from reduced paternal care whereas females suffer from it. By investigating penduline tits Remiz pendulinus in nature, we show that parental conflict may be symmetric between sexes. In this small passerine a single female (or male) cares for the offspring, whereas about 30% of clutches are deserted by both parents. Deserting parents enhance their RS by obtaining multiple mates, and they reduce the RS of their mates due to increased nest failure. Unlike most other species, however, the antagonistic interests are symmetric in penduline tits, because both sexes enhance their own RS by deserting, whilst harming the RS of their mates. We argue that the strong antagonistic interests of sexes explain the high frequency of biparental desertion.

Directional changes in sexual size dimorphism in shorebirds, gulls and alcids.

The Charadrii (shorebirds, gulls and alcids) are one of the most diverse avian groups from the point of view of sexual size dimorphism, exhibiting extremes in both male-biased and female-biased dimorphism, as well as monomorphism. In this study we use phylogenetic comparative analyses to investigate how size dimorphism has changed over evolutionary time, distinguishing between changes that have occurred in females and in males. Independent contrasts analyses show that both body mass and wing length have been more variable in males than in females. Directional analyses show that male-biased dimorphism has increased after inferred transitions towards more polygynous mating systems. There have been analogous increases in female-biased dimorphism after transitions towards more socially polyandrous mating systems. Changes in dimorphism in both directions are attributable to male body size changing more than female body size. We suggest that this might be because females are under stronger natural selection constraints related to fecundity. Taken together, our results suggest that the observed variation in dimorphism of Charadrii can be best explained by male body size responding more sensitively to variable sexual selection than female body size.

Sexual size dimorphism in shorebirds, gulls, and alcids: the influence of sexual and natural selection.

Charadrii (shorebirds, gulls, and alcids) have an unusual diversity in their sexual size dimorphism, ranging from monomorphism to either male-biased or female-biased dimorphism. We use comparative analyses to investigate whether this variation relates to sexual selection through competition for mates or natural selection through different use of resources by males and females. As predicted by sexual selection theory, we found that in taxa with socially polygynous mating systems, males were relatively larger than females compared with less polygynous species. Furthermore, evolution toward socially polyandrous mating systems was correlated with decreases in relative male size. These patterns depend on the kinds of courtship displays performed by males. In taxa with acrobatic flight displays, males are relatively smaller than in taxa in which courtship involves simple flights or displays from the ground. This result remains significant when the relationship with mating system is controlled statistically, thereby explaining the enigma of why males are often smaller than females in socially monogamous species. We did not find evidence that evolutionary changes in sexual dimorphism relate to niche division on the breeding grounds. In particular, biparental species did not have greater dimorphism in bill lengths than uniparental species, contrary to the hypothesis that selection for ecological divergence on the breeding grounds has been important as a general explanation for patterns of bill dimorphism. Taken together, these results strongly suggest that sexual selection has had a major influence on sexual size dimorphism in Charadrii, whereas divergence in the use of feeding resources while breeding was not supported by our analyses.

A dynamic game-theoretic model of parental care.

We present a model in which members of a mated pair decide whether to care for their offspring or desert them. There is a breeding season of finite length during which it is possible to produce and raise several batches of offspring. On deserting its offspring, an individual can search for a new mate. The probability of finding a mate depends on the number of individuals of each sex that are searching, which in turn depends upon the previous care and desertion decisions of all population members. We find the evolutionarily stable pattern of care over the breeding season. The feedback between behaviour and mating opportunity can result in a pattern of stable oscillations between different forms of care over the breeding season. Oscillations can also arise because the best thing for an individual to do at a particular time in the season depends on future behaviour of all population members. In the baseline model, a pair splits up after a breeding attempt, even if they both care for the offspring. In a version of the model in which a pair stays together if they both care, the feedback between behaviour and mating opportunity can lead to more than one evolutionarily stable form of care.

Song, sexual selection, and a song control nucleus (HVc) in the brains of European sedge warblers.

Female sedge warblers select males that have more complex songs as mates. This study tests two predictions concerning HVc, a telencephalic nucleus that is essential for song learning and production: first, that males with more complex songs will have a larger HVc, and second that males who pair successfully will have a larger HVc than unpaired males. Data on song composition and pairing status were collected from wild sedge warblers breeding in Hungary. We found significant positive correlations between three song attributes (repertoire size, song complexity, and song length) and the size of HVc. Males that paired successfully also had more complex songs (repertoire size and song complexity, though not song length) than males that did not. However, we find no direct evidence that males who paired successfully had a larger HVc than unpaired males. These findings are discussed in relation to the possible functions of HVc and also to current views on sexual selection and the evolution of the song control pathway.

Trade-off between mating opportunities and parental care: brood desertion by female Kentish plovers.

Why do some parents care for their young whereas others divorce from their mate and abandon their offspring? This decision is governed by the trade-off between the value of the current breeding event and future breeding prospects. In the precocial Kentish plover Charadrius alexandrinus females frequently, but not always, abandon their broods to be cared for by their mate, and seek new breeding partners within the same season. We have shown previously that females' remating opportunities decline with date in the season, so brood desertion should be particularly favourable for early breeding females. However, the benefits are tempered by the fact that single-parent families have lower survival expectancies than those where the female remains to help the male care for the young. We therefore tested the prediction that increasing the value of the current brood (by brood-size manipulation) should increase the duration of female care early in the season, but that in late breeders, with reduced remating opportunities, desertion and thus the duration of female care should be independent of current brood size. These predictions were fulfilled, indicating that seasonally modulated trade-offs between current brood value and remating opportunities can be important in the desertion decisions of species with flexible patterns of parental care.

Multiple patterns of parental care.

Many animals show multiple patterns of parental care, where more than one of the four basic patterns (biparental care, uniparental care by males or females, or no care) is present within a single population during a single breeding season. We consider three reasons for the existence of multiple patterns of parental care: (1) mixed-strategy behaviours; (2) time-dependent behaviour with parents changing their care decision during the breeding season; and (3) quality differences between individuals leading to different care decisions being made depending on the qualities of both parents. The basic framework we use to investigate these is a two-stage game-theoretical model, and we highlight the importance of including feedback between the parental care decisions made by population members and the probability that a deserting individual will find a new mate. Including this feedback may introduce a nonlinear dependence of the fitness payoffs on the frequencies with which the pure strategies ('care' and 'desert') are played by each of the sexes. This can have important consequences for the existence of evolutionarily stable strategies (ESSs). For example, mixed-strategy ESSs may exist (an outcome forbidden if the feedback is not included) and, in one model, the feedback also prevents uniparental care by either sex from being evolutionarily stable. We also point out that decisions made by animals without dependent offspring can have important consequences for observed parental care behaviour. Copyright 1999 The Association for the Study of Animal Behaviour.