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.     

Female plumage spottiness signals parasite resistance in the barn owl (Tyto alba)

The hypothesis that extravagant ornaments signal parasite resistancehas received support in several species for ornamented malesbut more rarely for ornamented females. However, recent theorieshave proposed that females should often be under sexual selection,and therefore females may signal the heritable capacity toresist parasites. We investigated this hypothesis in the sociallymonogamous barn owl, Tyto alba, in which females exhibit on average more and larger black spots on the plumage than males,and in which males were suggested to choose a mate with respectto female plumage spottiness. We hypothesized that the proportionof the plumage surface covered by black spots signals parasiteresistance. In line with this hypothesis, we found that theectoparasitic fly, Carnus hemapterus, was less abundant onyoung raised by more heavily spotted females and those flieswere less fecund. In an experiment, where entire clutches werecross-fostered between nests, we found that the fecundity ofthe flies collected on nestlings was negatively correlatedwith the genetic mother's plumage spottiness. These resultssuggest that the ability to resist parasites covaries with theextent of female plumage spottiness. Among females collecteddead along roads, those with a lot of black spots had a smallbursa of Fabricius. Given that parasites trigger the developmentof this immune organ, this observation further suggests thatmore spotted females are usually less parasitized. The same analyses performed on male plumage spottiness all provided non-significant results. To our knowledge, this study is the first one showingthat a heritable secondary sexual characteristics displayedby females reflects parasite resistance.     

Melanin, carotenoid and structural plumage ornaments: information content and role in great tits Parus major

The importance of plumage colour as an indicator of individual quality and the basis of sexual selection has long been recognized. Of the three generally distinguished classes of plumage colours, melanin-based ornaments are traditionally considered to provide less reliable information than carotenoid-based traits. However, the role of structural ornaments in multiple signalling systems has rarely been examined, and no study has compared the information content and role of the three ornament types simultaneously. Here we investigated three plumage ornaments in great tits Parus major : the size of the melanin-based breast stripe, the carotenoid-based colour of the yellow breast and the structurally based reflectance properties of the black crown. We worked on both the mechanistic and the functional levels. First, we assessed the dependence of ornaments on body condition during moult using ptilochronology. Second, we estimated assortative mating for these traits, as a measure of mutual sexual selection. Only the spectral attributes of crown feathers correlated with body condition during moult. However, breast stripe size was related to age, while the brightness of the yellow breast indicated body size. Relative crown ultraviolet reflectance was much higher in males than in females. Assortative mating was strongest for crown ultraviolet reflectance, but composite measures suggest that a system of multiple sexually selected traits with different information content may work in this population. These data support the accumulating evidence that the condition-dependence of melanin and carotenoid coloration is not qualitatively different. They also suggest that more research should target the reflectance properties of dark plumage areas in general, and ultraviolet crown ornamentation in tits in particular.     

Feather ornaments are dynamic traits in the Great Tit Parus major

In behavioural studies it has been common to quantify plumage colours or ornaments over a range of dates and link them to fitness characteristics without accounting for seasonal changes in these traits. Such changes are likely to be widespread among birds, yet we lack assessments of this variability within individuals. We studied both within‐ and between‐individual temporal changes in Great Tit Parus major ornaments, specifically the melanin‐based black breast stripe and the pigment‐free white cheek patch. During the non‐breeding season both ornaments varied. In juveniles and adult females, the area of the breast stripe first rose and then, from near the end of December, decreased. In adult males there was a linear decrease. In the cheek patch, the irregularity of the cheek borders showed either a linear (adults) or a non‐linear (juveniles) increase as the season progressed. In individuals repeatedly sampled during the same winter, the decrease in the size of the breast stripe was larger for males than females and there was an overall decrease in the regularity of the cheek borders. There was no relationship between the size of the breast stripe and the white cheek patch irregularities or the cheek patch area. These results imply that more attention should be paid to quantification, within individuals, of the components of expression of phenotypic traits. In addition, we suggest that further research should focus on explaining the causes and functions of ornament change.     

Effect of an ectoparasite on lay date, nest-site choice, desertion, and hatching success in the great tit (Pants major)

Ectoparasites are common in most bird species, but experimentalevidence of their effects on life-history traits is scarce.We investigated experimentally the effects of the hematophagoushen flea (Ceratophyllus gallinae) on timing of reproduction,nest-site choice, nest desertion, clutch size, and hatchingsuccess in the great tit (Parus major). When great tits wereoffered a choice on their territory between an infested anda parasite-free nest-box, they chose the one without parasites.When there was no choice, the great tits in a territory containingan infested nest-box delayed laying the clutch by 11 days ascompared with the birds that were offered a parasite-free nestingopportunity. The finding that there was no difference in phenotypictraits related to dominance between the birds nesting in infestedboxes and birds nesting in parasite-free boxes suggests thatthe delay is not imposed by social dominance. Nest desertionbetween laying and shortly after hatching was significandy higherin infested nests. There was no difference between infestedand parasite-free nests in clutch size, but hatching successand hence brood size at hatching were significantly smallerin infested nests. Nest-box studies of great tits have beenseminal in the development of evolutionary, ecological, andbehavioral theory, but recently a polemic has arisen in theliterature about the validity of the conclusions drawn fromnest-box studies where the naturally occurring, detrimentalectoparasites are eliminated by the routine removal of old nestsbetween breeding seasons. Our study suggests that this criticismis valid and that the evaluation of the effects of ectoparasitesmay improve our understanding of behavioral traits, life-historytraits, or population dynamics     

Dietary mineral content influences the expression of melanin-based ornamental coloration

Many animals develop bold patches of black or brown colorationthat are derived from melanin pigments and serve as sexual orsocial signals. At present, there is much debate among behavioralecologists over whether melanin-based color signals are costlyto produce. Studies that have manipulated crude aspects of nutrition(i.e., total food intake) or health have generally found melanin-basedplumage ornaments to be less responsive to such factors thanother types of extravagant color (e.g., carotenoid or structuralbased). However, a recently advanced hypothesis argues thatlimited minerals in the diet, such as calcium (Ca), zinc (Zn),and iron (Fe), may serve to increase melanin pigment productionand maintain signal honesty. Here, I experimentally tested whethervariation in the calcium content of the diet affects the colorand extent of melanin-based plumage in male zebra finches (Taeniopygiaguttata). Calcium supplementation increased the size, but notdarkness, of the black breast plumage patch in fledgling andadult males; however, sexually selected, carotenoid-based redbeak coloration was not affected by the diet manipulation. Theseresults are the first to support the idea that acquisition ofminerals from the diet is a unique, limiting factor for theexpression of ornamental melanin coloration in animals.     

Inter-annual variation and information content of melanin-based coloration in female Eurasian kestrels

Competition for resources (e.g. mates or food) is the main evolutionary explanation for conspicuous ornaments in males, although this idea is not generalized in females. Whether or not the expression of melanic coloration is dependent on environmental conditions remains controversial. We studied three different melanin-based female traits in the Eurasian kestrel Falco tinnunculus , a sexually dichromatic species, for a period of 10 years: grey coloration in rump and tail and the width of the black subterminal tail band. We analysed these traits for within-individual variation among years, as well as their possible link with indices of quality, such as age, body size, and breeding performance. The results obtained demonstrate that female melanin-based coloration increased from yearlings to adults. In addition, the expression of female rump coloration covaried positively with the environmental conditions in the previous year (i.e. measured as clutch size at population level). Finally, we found a positive correlation between grey rump coloration and clutch size. These results suggest that the expression of rump coloration, a melanin-based trait, is environmentally constrained, and we propose that this character could function as an indicator of individual quality in female Eurasian kestrels.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 781–790.     

Spawning colouration,parasites and habitat selection in Salvelinus alpinus: initiating speciation by sexual selection?

The relationship between parasite infection and breeding ornamentation in an Arctic charr Salvelinus alpinus population was examined. Interrelationships between the intensities of parasites with different dietary transmission routes suggested that hosts were segregated by habitat and diet preferences. That is, intensities of parasites transmitted through intermediate hosts that share habitat were, in both sexes, positively interrelated. Negative interrelationships in the intensities of parasites transmitted through different hosts were found only in females. The intensity of breeding colouration was positively correlated with intensities of amphipod‐transmitted parasites in both sexes. Intensities of parasites transmitted through copepods showed no relationship to morphological or ornamental characters. Seen in the context of morphology and ornaments of previously described sympatric populations of Arctic charr, these relationships suggested that individual variation in niche background may provide a source for the initial variation in morphology and secondary sexual traits leading to sympatric speciation through sexual selection.     

Winter male plumage coloration correlates with breeding status in a cooperative breeding species

The function of colored ornaments is usually related to thesignaling of individual quality in intra- and intersexual interactions.In cooperative breeding species, where only a fraction of themale population access the breeding status and the other fractionhas the option to help breeding pairs, colored traits mightprovide the females with a reliable information on the qualityof potential mate. Males of the cooperative breeding azure-wingedmagpies (Cyanopica cyanus) display conspicuous blue plumagecoloration. Here we explored the role played by structural bluecoloration of males and the probability of becoming a breederor a helper. Birds were trapped during 4 consecutive years,and feather coloration was measured with a spectrometer. Malesthat became breeders had a more brilliant and saturated bluecoloration and showed a more violet hue in the nonbreeding periodcompared with birds that became helpers. Breeding males alsoshowed a seasonal decline in blueness, whereas the color propertiesof helpers were constant throughout the year. Blueness of individualstrapped in the nonbreeding period was positively correlatedwith body size and condition. These findings are consistentwith a scenario in which nonbreeding blue plumage colorationmay function as a signal of individual quality in the azure-wingedmagpie at the pair formation time and add to growing evidencesuggesting that the nonbreeding season appears particularlyimportant in impacting breeding roles in cooperative breedingbirds.     

Repeatability of mate choice in female red jungle fowl

We staged female mate choice trials between pairs of males andrepeated the process for each female to determine the repeatabilityof female preference for males in red jungle fowl (Gallus gallus)in the first and second half of the breeding season. We measuredmale morphological traits (the size and color of the comb andthe brightness of the hackle feathers) that females are knownto use in choosing a mate. In the first half of the breedingseason, females showed repeatability in their choices of matewith respect to the male's comb characters. Females did notshow a repeatable preference with respect to male hackle feathers,and we found no repeatability of mate choice in the second halfof the season. Females seem to primarily look at the male'scomb when choosing a mate, and other ornaments seem only ofsecondary importance.[Behav Ecol 7: 243-246 (1996)]     

Parasites differentially increase the degree of fluctuating asymmetry in secondary sexual characters

The degree of fluctuating asymmetry has been demonstrated to reflect the ability of individuals to cope with different kinds of environmental stress (Parsons 1990). Parasites and diseases are one kind of environmental stress which most individuals encounter during their lifetime. Parasites have also been suggested to play an important role in sexual selection and the development of ornaments, since the full expression of ornaments may reflect the ability of hosts to cope with the debilitating effects of parasites. Here I report for the first time that a parasite, the haematophagous tropical fowl mite Ornithonyssus bursa (Macronyssidae, Gamasida), directly affects the degree of fluctuating asymmetry in a secondary sexual character of its host, the elongated tail of the swallow Hirundo rustica (Aves: Hirundinidae). I experimentally manipulated the mite load of swallow nests during one season by either increasing or reducing the number of mites, or keeping nests as controls. The degree of fluctuating asymmetry was measured in the subsequent year after the swallows had grown new tail ornaments under the altered parasite regime. The degree of fluctuating asymmetry was larger at increasing levels of parasites for male tail length, but not for the length of the shortest tail feather or wing length or for tail and wing length in females. These results suggest that the degree of fluctuating asymmetry in tail ornaments, but not in other feather traits, reliably reveals the level of parasite infestation. This has important implications for the ability of conspecifics to use the size and the expression of ornaments in assessment of phenotypic quality and thus in sexual selection.     

The direction of mothers' and daughters' preferences and the heritability of male ornaments in red jungle fowl (Gallus gallus)

We used a breeding design involving 18 sires and 108 dams tostudy the heritabilities of male ornaments in red jungle fowl(Gallus gallus). Ornaments used by females to choose mates showedlow heritabilities, with the exception of comb and wattle measures.The general absence of heritability suggests that a geneticcovariance did not exist at the time of this study between mostmale ornaments and female preferences for those ornaments. Thisresult is contrary to a key prediction of the arbitrary or Fisherianhypothesis of sexual selection. Comb size and color are condition-dependenttraits that reflect short-term changes in health, and comb sizeof males was positively correlated with offspring weight. Ourresults are consistent with the expectation of good-genes hypothesesthat male ornaments reflect the ability of males to withstandenvironmental stresses.     

Sexual selection in sticklebacks in the field: correlates of reproductive, mating, and paternal success

Male sticklebacks display multiple ornaments, and these ornamentshave been shown to be preferred by females in laboratory experiments.However, few field data exist, and it is not known whether thesepreferences are simultaneously or sequentially operative ina single population. We report correlates of reproductive successin two stickleback populations that differ in their ecology,over several periods within their breeding season. In both populationslarger males had higher reproductive success, but not in all periodsof the breeding season. Reproductive success increased withredness of the throat only in the Wohlensee population, andonly in one period that was characterized by low average success.In the Wohlensee population, the parasitic worm Pomphorhynchuslaevis is abundant, and reproductive success decreased withthe presence of the parasite. In the Roche population, maleswith nests concealed in a plant had higher mating success. Thesenests were less likely to fail, suggesting that females preferredto spawn in concealed nests because of higher offspring survivorship.The different sexual traits appear to reveal different aspectsof male quality (multiple message hypothesis): females probablyfind large males attractive because of their higher paternalquality, but it seems more likely that red males are preferred forbetter genetic qualities. Females also discriminate on territoryquality, and male traits may be important in competition forthese territories. The correlates of reproductive success werenot consistent during the season, probably due to changes inthe availability of ripe females. Such fluctuating selectionpressures will contribute to the maintenance of genetic variationin sexual traits.     

Offspring sex ratio is related to male body size in the great tit (Parus major)

Sex allocation theory predicts that the allocation of resourcesto male and female function should depend on potential fitnessgain realized through investment in either sex. In the greattit (Parus major), a monogamous passerine bird, male resourceholdingpotential (RHP) and fertilization success both depend on malebody size (e.g., tarsus length) and plumage traits (e.g., breaststripe size). It is predicted that the proportion of sons ina brood should increase both with male body size and plumage traits,assuming that these traits show a father—offspring correlation. Thiswas confirmed in our study: the proportion of sons in the brood increasedsignificantly with male tarsus length and also, though not significantly,with the size of the breast stripe. A sex ratio bias in relationto male tarsus length was already present in the eggs because(1) the bias was similar among broods with and without mortalitybefore the nestlings' sex was determined, and (2) the bias remainedsignificant when the proportion of sons in the clutch was conservativelyestimated, assuming that differential mortality before sex determinationcaused the bias. The bias was still present among recruits.The assumption of a father—offspring correlation was confirmedfor tarsus length. Given that both RHP and fertilization successof male great tits depend on body size, and size of father andoffspring is correlated, the sex ratio bias may be adaptive.     

Status signalling in male but not in female Eurasian Tree Sparrows Passer montanus

Male ornaments, such as plumage coloration, frequently serve as signals. The signalling function of similar ornaments in females has, however, received much less attention despite the fact that conspicuousness of their ornaments is often comparable to those of males. In this study we tested the signalling function of a plumage trait present in both sexes in the Eurasian Tree Sparrow Passer montanus. The black throat patch has been repeatedly found to have a signal function in the closely related House Sparrow Passer domesticus, where only males bear the ornamental trait. However, the function of the black throat patch in the females of Passer species that have sexually monomorphic ornament expression has never, to our knowledge, been considered. We investigated the outcomes of aggressive encounters in foraging flocks of free‐living Tree Sparrows, and assessed whether throat patch size and measurements of body size predicted fighting success in these flocks. We found that male throat patch size predicted fighting success against both male and female opponents. However, female throat patch size did not correlate with fighting success against either sex. Among the morphological traits studied, wing length was the best predictor of fighting success in females. Our findings suggest a status signalling function of throat patch size in males but not in females, although further experimental studies are necessary to corroborate these correlative results.     

Testosterone, immunocompetence, and honest sexual signaling in male red grouse

The expression of sexual ornaments has been suggested to reliablyindicate individual quality, such as the ability to cope withparasites and diseases. The Immunocompetence Handicap Hypothesis(IHH) states that testosterone-dependent ornaments honestlysignal such quality because of physiological costs associatedwith testosterone, such as impaired immune function. We testedpredictions of the IHH both correlatively and experimentallyin red grouse Lagopus lagopus scoticus. Male grouse exhibitsupra-orbital red combs whose size is testosterone-dependent.We found that comb size was not correlated to infection intensityby two parasites (coccidia and the nematode Trichostrongylustenuis), but it was significantly positively correlated withcondition and T-cell-mediated immunity (the ability to mounta primary inflammatory response). We manipulated testosteroneby means of implants and re-caught males after a month to investigatethe effects on comb size, condition, immunity, and parasiteload. Males implanted with testosterone had increased comb size,lost more condition, and had lower T-cell-mediated immunitythan control males. Increased testosterone also resulted ina significant increase in coccidia infection intensity but hadno effect on T. tenuis burden. The results are consistent withpredictions of the IHH and suggest that comb size honestly indicatesimmunocompetence and males' ability to cope with certain parasites.Females could thus benefit from choosing mates based on theexpression of this sexual trait.     

Heterospecific mating preferences for a feather ornament in least auklets

Auklets (Alddae, Aethiini) include five species of small, sociallymonogamous, sexually monomorphic seabirds that display a varietyof feather and bare-part ornaments during the breeding season.Previous experimental work on two auklet species has demonstratedthat some ornaments are likely to be favored by sexual selectionbecause mutual male and female mating preferences benefit individualswith the most elaborate expression of these traits. In thisstudy we experimentally investigated whether naturally crestlessleast auklets Aethia pusilla have a maring preference for foreheadcrests similar to the most prominent ornament of two other species,crested A. cristatella and whiskered auklets A. pygmaea. Ourobjective was to investigate the function of this ornament asa species-recognition mechanism or as a product of one or moreof three proposed sexual selection models that address the originof elaborate traits and preferences. During the experiment,least auklets reacted to realistic models equipped with artificialforehead crests with approximately an order of magnitude morefrequent sexual displays and greater interest, consistent withthe idea that they have a mating preference for crests, eventhough they do not naturally express this ornament This heterospecificpreference also favored large crest size. These results refutethe possibility that least auklet forehead ornamentation alonedetermines species recognition at present Among models of sexualselection considered, the results are consistent with the sensoryexploitation model, although this could not be established unequivocallybecause a viability indicator or Fisherian mechanism could havebeen involved if least auklets had an ancestor with a foreheadcrest.     

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.     

Temperature and development in host-parasite relationships

Summary The effects of temperature on growth and development of the cabbage butterfly, Pieris rapae, and three wasp parasites: Apanteles rubecula, Apanteles glomeratus and Pteromalus puparum in Vancouver, Canada, and Canberra, Australia, are examined. We compare the estimates of temperature threshold for development and the number of degree-days above this threshold required to complete development for the immature stages of all species in both localities. Developmental patterns of both the host and its parasites differ between localities. Within the range of temperatures likely to be experienced during the host's breeding season, Australian parasites have longer generation times than their host at low temperatures and shorter generation times at high temperatures. Canadian parasites have shorter generation times, relative to the host, at all temperatures. This may be necessitated by the shorter breeding season available to the Canadian parasites.Besides temperature, parasite development is affected by host size and, in the gregarious species, parasite density. Host larval development is retarded by both Apanteles.All parasites are smaller at higher temperatures and males are smaller than females, but size is also affected by host size and parasite density.Although parasite size, and consequently fecundity, varies greatly, parasites experiencing similar temperatures will have closely similar developmental periods. The ecological significance of these developmental responses is discussed.     

No evidence for long‐term effects of reproductive effort on parasite prevalence in great tits Parus major

Allocation of resources between the life history traits reproduction and parasite defence are expected because both are energetically costly. Experimental evidence for such allocation has been found in short‐term effects of reproduction on parasite prevalence or immune function. However, there is increasing evidence for long‐term negative effects of reproductive effort on individuals. This study investigates whether long‐term effects of reproductive effort on parasite prevalence exist. Brood sizes of great tits Parus major were experimentally altered in one breeding season and in the subsequent breeding season the prevalence of three parasites types (blood parasites, ticks and fleas) on the surviving parents were investigated. We detected no long‐term effects of brood size manipulation on the prevalence of parasites in the next year and therefore provide no evidence for inter‐seasonal effects of reproductive effort on parasite prevalence. The post hoc level of statistical power was reasonable for effects on blood parasite and flea prevalence, but low for effects on tick prevalence.