Physiological stress links parasites to carotenoid‐based colour signals

Vertebrates commonly use carotenoid‐based traits as social signals. These can reliably advertise current nutritional status and health because carotenoids must be acquired through the diet and their allocation to ornaments is traded‐off against other self‐maintenance needs. We propose that the coloration more generally reveals an individual’s ability to cope with stressful conditions. We tested this idea by manipulating the nematode parasite infection in free‐living red grouse (Lagopus lagopus scoticus) and examining the effects on body mass, carotenoid‐based coloration of a main social signal and the amount of corticosterone deposited in feathers grown during the experiment. We show that parasites increase stress and reduce carotenoid‐based coloration, and that the impact of parasites on coloration was associated with changes in corticosterone, more than changes in body mass. Carotenoid‐based coloration appears linked to physiological stress and could therefore reveal an individual’s ability to cope with stressors.     

Testing the role of parasites in driving the cyclic population dynamics of a gamebird

The role of parasites in regulating populations has been the subject of debate. We tested whether parasites caused population cycles in red grouse by manipulating parasite intensities in four, paired 1 km² study areas during cyclic population declines over 4 years. Parasite reductions led to (1) larger grouse broods, (2) higher population densities in both autumn and spring, (3) reduced autumn population declines in one of two regions, and (4) reduced spring declines, but only in the first year. We infer that a single trophic interaction between a parasite and its host does not explain cyclic dynamics in spring breeding density in this species, although it contributed to the start of a cyclic decline. Another process was operating to drive the populations down. Together with our other results these findings emphasize that both trophic and intrinsic processes may act within populations to cause unstable dynamics.     

Elevated spring testosterone increases parasite intensity in male red grouse

The expression of testosterone-dependent sexual traits mightsignal the ability of their bearers to cope with parasite infections.According to the immunocompetence handicap hypothesis (IHH),such signals would be honest because physiological costs oftestosterone, such as a reduced ability to control parasiteinfections, would prevent cheating. We tested whether testosteronewould affect the outcome of a standardized parasite challengein red grouse, using a main parasite of the species, the nematodeTrichostrongylus tenuis. We caught males in spring, removedtheir nematode parasites, and implanted them with testosteroneor empty implants, as controls. After 1 month, they were reinfectedwith a standard dose of infective T. tenuis parasites. Whenchallenged, testosterone males had relatively less globulinrelative to albumin plasma proteins than control males, an indicationthat they had experienced increased physiological stress. Testosterone-treatedmales had significantly more T. tenuis parasites than controlsin the next autumn and also had more coccidia and lost moreweight than controls. Testosterone-treated males neverthelessbenefited from their elevated spring testosterone: they hadbigger sexual ornaments than controls both in spring and autumn,and they tended to have a higher pairing and breeding successthan controls. Our results supported the IHH in showing thatelevated testosterone impaired the ability of males to copewith a standardized challenge by a dominant parasite. Testosteronethus plays a key role in mediating trade-offs between reproductiveactivities and parasite defense, and testosterone-dependentcomb size might honestly signal the ability of red grouse tocontrol T. tenuis infection.     

Nematode parasites reduce carotenoid-based signalling in male red grouse

Carotenoids determine the yellow-red colours of many ornaments, which often function as signals of quality. Carotenoid-based signalling may reliably advertise health and should be particularly sensitive to parasite infections. Nematodes are among the commonest parasites of vertebrates, with well-documented negative effects on their hosts. However, to date, little is known about the effects that these parasites may have on carotenoid-based signalling. Tetraonid birds (grouse) exhibit supra-orbital combs, which are bright integumentary ornaments pigmented by carotenoids. We tested the effect of the nematode parasite Trichostrongylus tenuis on signalling in free-living male red grouse Lagopus lagopus scoticus. We show that experimentally reduced nematode infection increases plasma carotenoid concentration and comb redness, demonstrating for the first time that nematodes can influence carotenoid-based signals.     

Honest sexual signalling mediated by parasite and testosterone effects on oxidative balance

Extravagant ornaments evolved to advertise their bearers'' quality, the honesty of the signal being ensured by the cost paid to produce or maintain it. The oxidation handicap hypothesis (OHH) proposes that a main cost of testosterone-dependent ornamentation is oxidative stress, a condition whereby the production of reactive oxygen and nitrogen species (ROS/RNS) overwhelms the capacity of antioxidant defences. ROS/RNS are unstable, very reactive by-products of normal metabolic processes that can cause extensive damage to key biomolecules (cellular proteins, lipids and DNA). Oxidative stress has been implicated in the aetiology of many diseases and could link ornamentation and genetic variation in fitness-related traits. We tested the OHH in a free-living bird, the red grouse. We show that elevated testosterone enhanced ornamentation and increased circulating antioxidant levels, but caused oxidative damage. Males with smaller ornaments suffered more oxidative damage than those with larger ornaments when forced to increase testosterone levels, consistent with a handicap mechanism. Parasites depleted antioxidant defences, caused oxidative damage and reduced ornament expression. Oxidative damage extent and the ability of males to increase antioxidant defences also explained the impacts of testosterone and parasites on ornamentation within treatment groups. Because oxidative stress is intimately linked to immune function, parasite resistance and fitness, it provides a reliable currency in the trade-off between individual health and ornamentation. The costs induced by oxidative stress can apply to a wide range of signals, which are testosterone-dependent or coloured by pigments with antioxidant properties.     

The direct and indirect effects of predation by Hen Harriers Circus cyaneus on trends in breeding birds on a Scottish grouse moor

Two phases of an experimental reduction in management at Langholm Moor in southwest Scotland provided an insight into factors that determined trends in the abundance of moorland birds. In 1992 the historical control of breeding Hen Harriers Circus cyaneus stopped and in 2000 grouse moor management was discontinued. Golden Plover Pluvialis apricaria , Lapwing Vanellus vanellus , Curlew Numenius arquata and Red Grouse Lagopus lagopus scoticus declined, whilst Carrion Crow Corvus corone and Snipe Gallinago gallinago increased. Hen Harriers increased from two to 20 breeding females, then declined back to two. Lapwing abundance was positively associated with that of Hen Harriers, and moorland passerines (Skylark Alauda arvensis , Meadow Pipit Anthus pratensis and Stonechat Saxicola torquata ) were negatively associated. Golden Plover, Lapwing, Curlew, Red Grouse, Skylark and Hen Harrier were more abundant when the moor was managed for grouse, whilst Carrion Crow, a common predator of clutches of ground-nesting birds, increased during the second half when management ceased. Increased Crow numbers, together with an increase in Red Foxes Vulpes vulpes , probably contributed to the observed bird declines.     

Environmental heterogeneity influences the reliability of secondary sexual traits as condition indicators

Numerous studies have shown positive associations between ornaments and condition, as predicted by indicator models of sexual selection. However, this idea is continuously challenged by opposite results, which reveal our lack of full understanding of how sexual selection works. Environmental heterogeneity may explain such inconsistencies, but valid field tests of this idea are currently lacking. We first analysed the relationship between condition and ornament expression from nine populations over 7 years in a wild bird, the red grouse Lagopus lagopus scoticus. We then manipulated male aggressiveness at the population level by means of testosterone implants in a replicated field experiment. We found that the relationship between condition and ornamentation varied greatly between environments and became stronger when environmental conditions (ECs) were worse or when aggressiveness in the population was experimentally increased. Some ornaments may therefore reliably advertise a better condition only in adverse ECs. Considering environmental heterogeneity can help reconcile conflicting findings regarding the reliability of ornaments as indicators of condition and will help our understanding of sexual selection processes.     

Temporal changes in kin structure through a population cycle in a territorial bird, the red grouse Lagopus lagopus scoticus

Populations of red grouse ( Lagopus lagopus scoticus ) undergo regular multiannual cycles in abundance. The 'kinship hypothesis' posits that such cycles are caused by changes in kin structure among territorial males producing delayed density-dependent changes in aggressiveness, which in turn influence recruitment and regulate density. The kinship hypothesis makes several specific predictions about the levels of kinship, aggressiveness and recruitment through a population cycle: (i) kin structure will build up during the increase phase of a cycle, but break down prior to peak density; (ii) kin structure influences aggressiveness, such that there will be a negative relationship between kinship and aggressiveness over the years; (iii) as aggressiveness regulates recruitment and density, there will be a negative relationship between aggressiveness in one year and both recruitment and density in the next; (iv) as kin structure influences recruitment via an affect on aggressiveness, there will be a positive relationship between kinship in one year and recruitment the next. Here we test these predictions through the course of an 8-year cycle in a natural population of red grouse in northeast Scotland, using microsatellite DNA markers to resolve changing patterns of kin structure, and supra-orbital comb height of grouse as an index of aggressiveness. Both kin structure and aggressiveness were dynamic through the course of the cycle, and changing patterns were entirely consistent with the expectations of the kinship hypothesis. Results are discussed in relation to potential drivers of population regulation and implications of dynamic kin structure for population genetics.     

Intra-sexual competition alters the relationship between testosterone and ornament expression in a wild territorial bird

In a reliable signalling system, individual quality is expected to mediate the costs associated with ornamental displays, with relatively lower costs being paid by individuals of higher quality. These relative costs should depend not only on individual quality, but also on levels of intra-sexual competition. We explored the current and delayed effects that testosterone implants have on bird ornamentation in populations with contrasted population densities, as a proxy for intra-sexual competition. In a replicated experiment, we manipulated testosterone in 196 yearling male red grouse Lagopus lagopus scoticus in autumn in populations of high and low levels of intra-sexual competition. Males were assigned to one of three exogenous testosterone (T) treatments: empty implants (T0), small T implants (T1) or larger T implants (T2). We monitored subsequent changes in testosterone levels, ornament size and carotenoid-based colouration, carotenoid levels and body condition from autumn to spring. Testosterone implants increased testosterone levels, comb redness and comb size, and decreased body condition but these effects depended on levels of intra-sexual competition. Specifically, T2-implanted birds increased testosterone levels and comb size more, and reduced body condition more, in populations where intra-sexual competition was low. In the following spring, testosterone levels of T2-treated birds kept increasing in populations where intra-sexual competition was high but not in populations where intra-sexual competition was low. Our results highlight that levels of intra-sexual competition alter the relationship between testosterone levels and ornament expression, influencing their condition-dependence; they also indicate that the outcome of standard hormone manipulation conducted in free-living animals vary depending on the population context.     

Condition‐dependence,pleiotropy and the handicap principle of sexual selection in melanin‐based colouration

The signalling function of melanin‐based colouration is debated. Sexual selection theory states that ornaments should be costly to produce, maintain, wear or display to signal quality honestly to potential mates or competitors. An increasing number of studies supports the hypothesis that the degree of melanism covaries with aspects of body condition (e.g. body mass or immunity), which has contributed to change the initial perception that melanin‐based colour ornaments entail no costs. Indeed, the expression of many (but not all) melanin‐based colour traits is weakly sensitive to the environment but strongly heritable suggesting that these colour traits are relatively cheap to produce and maintain, thus raising the question of how such colour traits could signal quality honestly. Here I review the production, maintenance and wearing/displaying costs that can generate a correlation between melanin‐based colouration and body condition, and consider other evolutionary mechanisms that can also lead to covariation between colour and body condition. Because genes controlling melanic traits can affect numerous phenotypic traits, pleiotropy could also explain a linkage between body condition and colouration. Pleiotropy may result in differently coloured individuals signalling different aspects of quality that are maintained by frequency‐dependent selection or local adaptation. Colouration may therefore not signal absolute quality to potential mates or competitors (e.g. dark males may not achieve a higher fitness than pale males); otherwise genetic variation would be rapidly depleted by directional selection. As a consequence, selection on heritable melanin‐based colouration may not always be directional, but mate choice may be conditional to environmental conditions (i.e. context‐dependent sexual selection). Despite the interest of evolutionary biologists in the adaptive value of melanin‐based colouration, its actual role in sexual selection is still poorly understood.     

Condition‐dependence and sexual ornamentation: Effects of immune challenges on a highly sexually dimorphic grasshopper

Sexual ornaments contribute substantially to phenotypic diversity and it is particularly relevant to understand their evolution. Ornaments can assume the function of signals‐of‐quality that the choosy sex uses to evaluate potential mating partners. Often there are no obvious direct benefits and investment into mate choice is primarily rewarded by beneficial alleles that are inherited to the offspring. Inter‐sexual communication via sexual ornaments requires honesty of the sexual signal, yet the question of what maintains honesty remains only partially solved. One solution is that honesty is maintained by trait expression being dependent on individual condition, since condition‐dependent trait expression offers an effectively inexhaustible source of genetic variability. Here we test in the highly sexually dimorphic club‐legged grasshopper Gomphocerus sibiricus if putative sexual ornaments, in particular the striking front‐leg clubs, are more strongly affected by a lipopolysaccharide (LPS) immune challenge than putatively not sexually selected traits. Our results show overall little condition‐dependent expression of morphological and song traits, with sexually selected traits exhibiting effects comparable to nonsexually selected traits (with the possible exception of stridulatory file length and syllable‐to‐pause ratio in advertisement songs). Interestingly, field observations of individuals of lethally parasitized individuals suggest that a very strong environmental challenge can specifically affect the expression of the front‐leg clubs. The presence of 1% of males in natural populations with missing or heavily deformed clubs plus 5% with minor club deformations furthermore indicate that there are risks associated with club development during final ecdysis and this might act as a filter against deleterious alleles.     

An appraisal of how the vitamin A‐redox hypothesis can maintain honesty of carotenoid‐dependent signals

The vitamin A‐redox hypothesis provides an explanation for honest signaling of phenotypic quality by carotenoid‐dependent traits. A key aspect of the vitamin A‐redox hypothesis, applicable to both yellow and red coloration, is the hypothesized negative feedback of tightly regulated Vitamin A plasma levels on the enzyme responsible for sequestering both Vitamin A and carotenoids from the gut. We performed a meta‐analysis and find that vitamin A levels are positively related to carotenoid plasma levels (r = 0.50, P = 0.0002). On the basis of this finding and further theoretical considerations, we propose that the vitamin A‐redox hypothesis is unlikely to explain carotenoid‐dependent honest signaling.     

Rising burden of immature sheep ticks (Ixodes ricinus) on red grouse (Lagopus lagopus scoticus) chicks in the Scottish uplands

The sheep tick Ixodes ricinus (L.) (Acari: Ixodidae) is an ectoparasite of major economic and pathogenic importance in Scotland. Its distribution in the Scottish uplands is assumed to be governed by the abundance and distribution of its definitive hosts (deer and sheep) and climatic variables such as temperature and rainfall. As the numbers of its major host in Scotland, red deer, have increased dramatically and climatic conditions have become more favourable, the level of parasitism could have been expected to rise. We use data gathered from tick counts on over 4000 red grouse chicks Lagopus lagopus scoticus Latham (Galliformes: Tetraonidae) in various experiments over the past 19 years to ascertain whether the intensity and prevalence of parasitism has been increasing. From 1985 to 2003 the average tick burden of a parasitized red grouse chick has grown from 2.60 +/- 1.12 ticks per chick to 12.71 +/- 1.44. Over this period the percentage of chicks of a given brood parasitized has also increased from 4 +/- 2% to 92 +/- 3%. The possible implications of this increase in parasitism for red grouse production are discussed.     

Habitat constraints on carotenoid‐based coloration in a small euryhaline teleost

Display of bright and striking color patterns is a widespread way of communication in many animal species. Carotenoid‐based coloration accounts for most of the bright yellow, orange, and red displays in invertebrates, fish, amphibians, reptiles, and birds, being widely considered a signal of individual health. This type of coloration is under the influence of several factors, such as sexual selection, predator pressure, pigment availability, and light transmission. Fish offer numerous examples of visual communication by means of color patterns. We used a small cyprinodontid fish, Aphanius fasciatus (Valenciennes, 1821), as a model species to assess habitat constraints on the color display in male caudal fin. Populations from natural and open/closed artificial habitats were tested for differences in the pigmentation of caudal fins. The most important factors explaining the intensity of coloration were the habitat type and the chlorophyll concentration in the sediment, followed by water turbidity; yellow fins were observed in natural habitats with low chlorophyll concentration and high water turbidity, while orange fins occurred in artificial habitats with high chlorophyll concentration and low turbidity. Furthermore, A. fasciatus in artificial habitats showed a higher somatic and a lower reproductive allotment with respect to natural habitats, according to the existing literature on the species. Furthermore, in closed artificial habitats, where the most intense reddish coloration of caudal fins was observed, a trade‐off between somatic growth and the coloration intensity of a carotenoid‐based sexual ornament has been observed; in these populations, intensity of caudal fin coloration was negatively related to the somatic allotment. Results of this study suggested how both the pigmentation of male's caudal fin and the life history strategies of the species are constrained by habitat characteristics.     

Sex and age differences in reflectance and biochemistry of carotenoid‐based colour variation in the great tit Parus major

The plumage coloration in great tits (Parus major) is the subject of much behavioural and ecophysiological research, yet there is a lack of analyses of the natural colour variation and its mechanisms. We used reflectance spectrometry and high‐performance liquid chromatography to explore individual, sexual and age‐related variation in carotenoid coloration and pigmentation, paramount to the often presumed, but rarely substantiated, costs and ‘honesty’ of carotenoid displays. In adults, we found that sex was the strongest predictor of ‘brightness’ (higher in males) and of ‘hue’ (longer wavelength in females). There was no sex difference in ‘carotenoid chroma’ or carotenoid content of feathers which also was unrelated to adult age (1 or 2+ years) and condition. Similar patterns were revealed for nestlings. Regarding the biochemical ‘signal content’, ‘carotenoid chroma’, but not ‘hue’, was significantly related to the carotenoid content (lutein and zeaxanthin) of feathers. These results refute the previously assumed exaggeration of carotenoid pigmentation in male great tits, and question the condition‐dependence of carotenoid coloration in this species. However, the sexual dimorphism in total reflectance or ‘brightness’, most likely due to melanins rather than carotenoids, may have implications for signalling or other adaptive explanations that need to be explored. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 758–765.     

Experimental stress during molt suggests the evolution of condition‐dependent and condition‐independent ornaments in the king penguin

Sexual selection and social selection are two important theories proposed for explaining the evolution of colorful ornamental traits in animals. Understanding signal honesty requires studying how environmental and physiological factors during development influence the showy nature of sexual and social ornaments. We experimentally manipulated physiological stress and immunity status during the molt in adult king penguins (Aptenodytes patagonicus), and studied the consequences of our treatments on colourful ornaments (yellow‐orange and UV beak spots and yellow‐orange auricular feather patches) known to be used in sexual and social contexts in this species. Whereas some ornamental features showed strong condition‐dependence (yellow auricular feather chroma, yellow and UV chroma of the beak), others were condition‐independent and remained highly correlated before and after the molt (auricular patch size and beak UV hue). Our study provides a rare examination of the links between ornament determinism and selection processes in the wild. We highlight the coexistence of ornaments costly to produce that may be honest signals used in mate choice, and ornaments for which honesty may be enforced by social mediation or rely on genetic constraints.     

Seasonal variation in male testosterone levels in a tropical bird with year‐round territoriality

Testosterone is important in mediating investment in competing activities such as territoriality, parental care, and maintenance behavior. Most studies of testosterone function have focused on temperate species and less is known about the role of testosterone in territoriality or variation in mating systems of tropical species. Results of studies of tropical species with year‐round territoriality indicate that territorial aggression during the non‐breeding season is maintained with low levels of testosterone, and increased levels of testosterone in males during the breeding season may increase mating opportunities or aid in competition for mates. We studied seasonal variation in testosterone levels of male Red‐throated Ant‐tanagers (Habia fuscicauda), a socially monogamous species with year‐round territoriality and with high levels of extra‐pair matings (41% of young), to determine if testosterone levels increased during the breeding season. We captured males during the non‐breeding and breeding seasons and collected blood samples for hormone analysis. We found that mean testosterone concentrations were low during the non‐breeding season (0.18 ± 0.05 [SD] ng/ml, range = 0.11–0.31 ng/ml), and significantly higher during the breeding season (2.37 ± 2.47 ng/ml, range = 0.14–6.28 ng/ml). Testosterone levels of breeding males were not related to aggression levels as measured by attack rates toward a stuffed decoy or singing rates during simulated territorial intrusions. These results suggest that the higher testosterone levels of breeding male Red‐throated Ant‐tanagers may be important in an extra‐pair mating context, possibly in display behavior or mate attraction, but additional study is needed to clarify the role of testosterone during the breeding season.