Life history, immunity, Peto's paradox and tumours in birds.

Cancer and tumours may evolve in response to life-history trade-offs between growth and duration of development on one hand, and between growth and maintenance of immune function on the other. Here, we tested whether (i) bird species with slow developmental rates for their body size experience low incidence of tumours because slow development allows for detection of rapid proliferation of cell lineages. We also test whether (ii) species with stronger immune response during development are more efficient at detecting tumour cells and hence suffer lower incidence of tumours. Finally, we tested Peto's paradox, that there is a positive relationship between tumour incidence and body mass. We used information on developmental rates and body mass from the literature and of tumour incidence (8468 birds) and size of the bursa of Fabricius for 7659 birds brought to a taxidermist in Denmark. We found evidence of the expected negative relationship between incidence of tumours and developmental rates and immunity after controlling for the positive association between tumour incidence and body size. These results suggest that evolution has modified the incidence of tumours in response to life history and that Peto's paradox may be explained by covariation between body mass, developmental rates and immunity.

Predator-prey interactions, flight initiation distance and brain size.

Prey avoid being eaten by assessing the risk posed by approaching predators and responding accordingly. Such an assessment may result in prey-predator communication and signalling, which entail further monitoring of the predator by prey. An early antipredator response may provide potential prey with a selective advantage, although this benefit comes at the cost of disturbance in terms of lost foraging opportunities and increased energy expenditure. Therefore, it may pay prey to assess approaching predators and determine the likelihood of attack before fleeing. Given that many approaching potential predators are detected visually, we hypothesized that species with relatively large eyes would be able to detect an approaching predator from afar. Furthermore, we hypothesized that monitoring of predators by potential prey relies on evaluation through information processing by the brain. Therefore, species with relatively larger brains for their body size should be better able to monitor the intentions of a predator, delay flight for longer and hence have shorter flight initiation distances than species with smaller brains. Indeed, flight initiation distances increased with relative eye size and decreased with relative brain size in a comparative study of 107 species of birds. In addition, flight initiation distance increased independently with size of the cerebellum, which plays a key role in motor control. These results are consistent with cognitive monitoring as an antipredator behaviour that does not result in the fastest possible, but rather the least expensive escape flights. Therefore, antipredator behaviour may have coevolved with the size of sense organs, brains and compartments of the brain involved in responses to risk of predation.

Testicular melanization has evolved in birds with high mtDNA mutation rates.

Melanin is mainly found in the integument of animals, but it also appears in several extracutaneous tissues. The presence of melanin in testes has been anecdotally reported in all vertebrate groups, but the causes and functions of this melanin remain unknown. Similar to other extracutaneous melanins, testicular melanin may protect male germ cells from oxidative stress. Given the high respiratory activity of spermatozoa, oxidative stress generated by mitochondrial dysfunction as a consequence of mtDNA mutations directly affects sperm viability. Thus, natural selection may favour testicular melanization in males of species with high historical mutation rates in the mitochondrial genome. Here, we tested this hypothesis using information on occurrence of testicular melanization and mutation accumulation as reflected by cytochrome b mtDNA base pair substitution rates in a large set of 134 species of birds, controlling for the confounding effects of body mass, reproductive activity and phylogeny. We found that testicular melanization has evolved in species with high rates of accumulated mitochondrial mutations and propose that this is an adaptive response related to the protective capacity of melanin against oxidative stress. In support of this hypothesis, testicular melanization was more frequently observed during the breeding season of birds (i.e. when spermatogenesis is likely to occur) than during reproductive inactivity. In contrast to other extracutaneous melanins whose abundance seems to reflect skin and coat colour, we did not find a correlation between the proportion of plumage coloured by melanins and occurrence of testicular melanization. Whereas future experimental studies should test these hypotheses, our study highlights for the first time that melanization patterns in animals may evolve as a response to historical mutation rates.

Historical mutation rates predict susceptibility to radiation in Chernobyl birds.

Extreme environmental perturbations are rare, but may have important evolutionary consequences. Responses to current perturbations may provide important information about the ability of living organisms to cope with similar conditions in the evolutionary past. Radioactive contamination from Chernobyl constitutes one such extreme perturbation, with significant but highly variable impact on local population density and mutation rates of different species of animals and plants. We explicitly tested the hypothesis that species with strong impacts of radiation on abundance were those with high rates of historical mutation accumulation as reflected by cytochrome b mitochondrial DNA base-pair substitution rates during past environmental perturbations. Using a dataset of 32 species of birds, we show higher historical mitochondrial substitution rates in species with the strongest negative impact of local levels of radiation on local population density. These effects were robust to different estimates of impact of radiation on abundance, weighting of estimates of abundance by sample size, statistical control for similarity in the response among species because of common phylogenetic descent, and effects of population size and longevity. Therefore, species that respond strongly to the impact of radiation from Chernobyl are also the species that in the past have been most susceptible to factors that have caused high substitution rates in mitochondrial DNA.

Why birds eat colourful grit: colour preferences revealed by the colour of gizzard stones.

Colour preferences from sexual or social contexts are assumed to have arisen owing to preferences for specific kinds of food, representing a sensory bias, but once colour preferences have evolved in a sexual context, they may also be expressed during foraging. We tested whether preferences for specific body colours (i.e. plumage and soft parts) were related to colour preferences for grit ingested by birds. Birds eat grit to facilitate break down of food by the gizzard, and this function is independent of the colour of grit, but depends on the physical properties of stones. Bird species were significantly consistent in colour of grit, and grit of different colours varied in prevalence among species, even when analyses were restricted to a sample from a single locality. There were positive correlations between presence of lilac and red grit in the gizzard and presence of sexually dichromatic lilac and red colour on the body. There was a positive correlation between red grit colour and red sexually monochromatic body colour. Bird species with many different sexual colours, but not sexually monochromatic colours on their body had many different colours of grit. Males had more lilac and red grit than females, with this effect differing among species, whereas that was not the case for grit of other colours. These findings are consistent with the sensory bias hypothesis that birds express preferences for grit of specific colours and a high diversity of colours related to sexual colouration of the body, even when the colour of such grit is only visible to the individual at the moment of ingestion.

Covariation between brain size and immunity in birds: implications for brain size evolution.

Parasitism can negatively affect learning and cognition, setting the scene for coevolution between brain and immunity. Greater susceptibility to parasitism by males may impair their cognitive ability, and relatively greater male investment in immunity could compensate for greater susceptibility to parasites, in particular when males have a relatively large brain. We analysed covariation between relative size of immune defence organs and brain in juvenile and adult birds. The relative size of the bursa of Fabricius and the spleen in adults covaried positively with relative brain size across bird species. The relative size of these two immune defence organs covaried with sex differences in relative size of the brain, indicating that the relationship between immune defence and brain size was stronger for males. In contrast, liver and heart size or sexual size dimorphism in size did not covary with immune defence. Thus, species in which males have relatively large brains also have relatively large immune defence organs.

The evolution of song repertoires and immune defence in birds.

Song repertoires (the number of different song types sung by a male) in birds provide males with an advantage in sexual selection because females prefer males with large repertoires, and females may benefit because offspring sired by preferred males have high viability. Furthermore, males with large repertoires suffer less from malarial parasites, indicating that a large repertoire may reflect health status. We hypothesize that sexual selection may cause a coevolutionary increase in parasite virulence and host immune defence because sexual selection increases the risk of multiple infections that select for high virulence. Alternatively, a female mate preference for healthy males will affect the coevolutionary dynamics of host-parasite interactions by selecting for increased virulence and hence high investment by hosts in immune function. In a comparative study of birds, repertoire size and relative size of the spleen, which is an important immune defence organ, were strongly, positively correlated accounting for almost half of the variance. This finding suggests that host-parasite interactions have played an important role in the evolution of song repertoires in birds.

Predation against birds with low immunocompetence.

Differences in the phenotypic characteristics between individuals falling prey to predators and conspecifics avoiding predation will reflect the intensity of selection on prey. If prey are generally in poor condition, we predicted that they should have an inferior health status in comparison to individuals dying for other reasons. We investigated this prediction for prey and conspecifics that did not die from predation by comparing the size of the spleen, which is an important immune defence organ reflecting one component of immunocompetence, using 18 species of passerine birds and domestic cat Felis catus predators as a model system. Prey had consistently smaller spleens than non-prey, implying that they had weak immune systems. The data set did not indicate that sex or age, month of death, body mass, body condition, liver mass, wing length or tarsus length differed significantly between prey and non-prey. Thus there was little evidence of confounding factors affecting the results. These observations indirectly suggest that disease and parasitism may play an important role in predator-prey interactions.

Sexual dimorphism in immune defense.

Sex differences in parasitism are common and may depend on sex differences in intensity of sexual competition, immunosuppression, or exposure to parasites. We used a large data set on the mass of two immune defense organs in birds (the bursa of Fabricius and the spleen) to test for consistent sex differences in immune defense. Males had a relative spleen mass that was consistently smaller, but more variable, than that of females across species of birds. A sex difference in the size of the spleen was not present among juveniles but was large and statistically significant among adults. The suppression of spleen mass in adult males increased with a measure of intensity of sexual selection: the frequency of extra-pair paternity. These findings suggest that sex differences in parasitism may arise as a consequence of sex differences in immune function, as mediated by sexual selection.