Hamilton-Zuk Hypothesis Research Articles

Infection by a fungal pathogen and mating behavior in Pacific treefrogs: a test of the Hamilton-Zuk hypothesis

Infection by a fungal pathogen and mating behavior in Pacific treefrogs: a test of the Hamilton-Zuk hypothesis

Lizard Dewlap Color and Malaria Infection: Testing the Hamilton-Zuk Hypothesis

The Hamilton-Zuk hypothesis indicates that parasites may have a negative effect on the appearance of sexual traits within an infected individual. Anolis sagrei, or brown anoles, are small invasive lizards common throughout Florida and many other areas where they have been introduced. The colorful dewlaps under the chins of males are used as a signal during territorial contests with other males and as an ornament to attract females. Anoles may be infected by the malaria parasite Plasmodium floridense. In this study, we investigated the relationship of malarial infection with dewlap color and spectral brightness of A. sagrei. We achieved this by capturing male brown anoles, taking blood samples to examine for malarial infection, and recording the color of their dewlaps. We found that the dewlaps of infected Anolis sagrei had duller coloration than the dewlaps of uninfected lizards. These results provide support for the Hamilton-Zuk hypothesis. Our results suggest that infection by P. floridense could potentially influence fitness of the lizards by reducing the expression of their color signals. Additional research on fitness effects of the malaria parasite on anoles is important for fully understanding this phenomenon.

Museum-Based Research on the Lice (Insecta: Phthiraptera) Infestations of Hummingbirds (Aves: Trochilidae)—Prevalence, Genus Richness and Parasite Associations

We documented the presence/absence of the eggs of Trochiloecetes, Trochiliphagus, and Leremenopon lice on over 50,000 hummingbird specimens (representing 348 species plus 247 additional subspecies) in four museums in the USA. (i) We provide sample estimates of infestation prevalence. (ii) Sample estimates of parasite genus richness increased with increasing host sample size. (iii) Host body mass did not correlate with parasite genus richness, even when controlled for sample size effects. (iv) The prevalence of Trochiliphagus and Trochiloecetes infestations did not correlate with host body mass, while the prevalence of Leremenopon exhibited a marginally significant positive correlation with host body mass. (v) The prevalence of Trochiliphagus and Leremenopon infestations correlated strongly and positively across host taxa (i.e., species or subspecies). (vi) The co-occurrence of Trochiliphagus and Trochiloecetes within the few largest host samples—i.e., within particular host taxa—was significantly more frequent than expected by chance. This latter association might indicate a true ecological relationship or, alternatively, might have emerged as an artifact of our sampling method. (vii) We found no relationship between host sexual size dimorphism and the prevalence of any of the three louse genera, contrary to the interspecific prediction of the Hamilton–Zuk hypothesis.

Is Color Related to Parasite Load in a Sexually Dichromatic Neotropical Toad?

Research on anuran parasites often focuses on the description and identification of parasites and demonstrating that parasitic infection can have deleterious effects on the health of amphibians. There is comparatively little research on how parasitism influences evolutionary dynamics such as sexual selection. Here, we explore anuran blood parasites with a focus on parasite-mediated sexual selection. The Hamilton–Zuk hypothesis posits that parasite–host coevolution drives sexual ornamentation of hosts, and that the degree of ornament expression honestly signals heritable parasite resistance. Although the Hamilton–Zuk hypothesis has received support in a number of animal taxa, it has received little attention in amphibians. Neotropical Yellow Toads (Incilius luetkenii) are sexually dichromatic toads with an unusual sexual ornament: males turn from cryptic brown to bright lemon yellow for a very short period during the brief breeding season. In this study, we identify blood parasites in male Neotropical Yellow Toads, and we investigate one component of the Hamilton–Zuk hypothesis by comparing skin color and body condition to blood parasite levels. We found four types of parasites. Apicomplexa and frog erythrocytic virus were the most common, infecting 73% and 46% of toads, respectively, whereas Nematoda and bacteria were found in 27% and 36% of toads, respectively. We found negative relationships between parasites and male color: males infected with fewer Apicomplexa and Nematoda had higher yellow saturation, and males with fewer Nematoda had longer-wavelength hue. In contrast, we found one positive relationship between parasites and male color: males infected with higher levels of frog erythrocytic virus had higher brightness. Our results suggest that parasites may influence sexual traits in this species, but that the relationship is complex. This research contributes to our understanding of amphibian host–parasite coevolution by demonstrating a relationship between parasites and host coloration.

Brighter is darker: the Hamilton–Zuk hypothesis revisited in lizards

Abstract Several studies of lizards have made an erroneous interpretation of negative relationships between spectral brightness and parasite load, and thus provided misleading support for the Hamilton–Zuk hypothesis (HZH). The HZH predicts that infected hosts will produce poorer sexual ornamentation than uninfected individuals as a result of energetic trade-offs between immune and signalling functions. To test whether there is a negative relationship between spectral brightness and pigment content in the skin of lizards, we used spectrophotometry to quantify the changes in spectral brightness of colour patches of two species after chemically manipulating the contents of orange, yellow and black pigments in skin samples. Carotenoids were identified using high-performance liquid chromatography. In addition, we compared the spectral brightness in the colour patches of live individuals with differential expression of nuptial coloration. Overall, the analyses demonstrated that the more pigmented the colour patch, the darker the spectrum. We provide a comprehensive interpretation of how variation in pigment content affects the spectral brightness of the colour patches of lizards. Furthermore, we review 18 studies of lizards presenting 24 intraspecific tests of the HZH and show that 14 (58%) of the tests do not support the hypothesis.

Genomic Insights Into the Molecular Basis of Sexual Selection in Birds

Sexual selection is a well-known biological process, yet the genomic basis and patterns of sexual selection are not fully understood. The extravagant ornamental plumage of peacock (Pavo cristatus) was instrumental in shaping Charles Darwin's theory of sexual selection and is considered to be an honest signal of its immunocompetence. Here, we used the recently generated draft genome sequence of peafowl (Pavo cristatus) and carried out a comparative analysis across 11 bird genomes that encompass a range of sexual selection and also had high-quality genomic and phenotypic data publically available to study the genomic basis of sexual selection. We found that varying degree of purifying selection was the predominant mechanism of action for sexual selection at the genome-wide scale and observed that sexual selection mostly influences genes regulating gene expression and protein processing. Specifically, the genome-wide phylogenetically corrected regression analysis supported the continuous or ongoing model of sexual selection. Genes involved in nucleic acid binding and gene expression regulation, including a specific regulator of sex-determination known as TRA2A to be under positive selection in the species with high post-copulatory sexual selection manifested as high sperm competition. We also detected specific feather-related and immune-related gene-pairs evolving under similar selection pressures across the 11 species, including peacock (Pavo cristatus), which is consistent with the Hamilton-Zuk hypothesis. The comparative genomics analysis of 11 avian taxa has provided new insights on the molecular underpinnings of sexual selection and identifies specific genomic regions for future in-depth analysis.

Genome Sequence of Peacock Reveals the Peculiar Case of a Glittering Bird.

The unique ornamental features and extreme sexual traits of Peacock have always intrigued scientists and naturalists for centuries. However, the genomic basis of these phenotypes are yet unknown. Here, we report the first genome sequence and comparative analysis of peacock with the high quality genomes of chicken, turkey, duck, flycatcher and zebra finch. Genes involved in early developmental pathways including TGF-β, BMP, and Wnt signaling, which have been shown to be involved in feather patterning, bone morphogenesis, and skeletal muscle development, revealed signs of adaptive evolution and provided useful clues on the phenotypes of peacock. Innate and adaptive immune genes involved in complement system and T-cell response also showed signs of adaptive evolution in peacock suggesting their possible role in building a robust immune system which is consistent with the predictions of the Hamilton–Zuk hypothesis. This study provides novel genomic and evolutionary insights into the molecular understanding toward the phenotypic evolution of Indian peacock.

The relationship between blood parasites and ornamentation depends on the level of analysis in the common yellowthroat

The Hamilton–Zuk hypothesis predicts that ornament expression is a signal of the ability of individuals to resist parasite infection. Thus, across a population (i.e. between‐individuals) more ornamented individuals should have lower levels of parasitism. Numerous studies have tested this prediction and the results are mixed. One reason for these conflicting results may be that many studies have examined this relationship at the between‐individual level, which may be affected by confounding factors such as selective mortality. Using within‐subject centering we examined the relationship between male ornamentation and avian blood parasites at both the between‐ and within‐individual levels. These relationships focus on differences in genetically‐based resistance to parasites and the trade‐off in resource allocation between parasite resistance and ornament expression within an individual, respectively. We studied male common yellowthroats Geothlypis trichas, which have two plumage ornaments, a yellow, carotenoid‐based bib (throat and chest) and a black, melanin‐based facial mask. Surprisingly, within‐individuals, an increase in parasitism between years was associated with an increase in mask size and, potentially, greater concentration of carotenoids in the yellow feathers. This suggests that males may be able to tolerate an increase in parasitism and still increase ornament expression. In contrast, ornamentation was not related to parasitism at the between‐individual level. Thus, our study revealed relationships between ornaments and parasitism at the within‐individual level that were not present at the between‐individual level. Our results highlight the importance of examining both within‐ and between‐individual relationships as correlations between variables, such as ornaments and parasites, may depend on the level of analysis (i.e. within‐ or between‐individuals).

A rare study from the wintering grounds provides insight into the costs of malaria infection for migratory birds

Malaria parasites can have strong effects on the population dynamics and evolution of migratory bird species. In many species, parasite transmission occurs on the wintering grounds, but studies to determine the consequences of infection have taken place during the breeding season, when malaria parasites circulate at chronic levels. We examined the predictors of malarial infections for great reed warblers during the northern winter in Africa, where active parasite transmission is thought to occur and naïve individuals experience acute infections. Counter to expectations, we found that winter infection intensities were lower than those encountered on the breeding grounds. One potential explanation is that reduced immune function during breeding allows parasites to persist at higher chronic intensities. We found no relationships between the incidence or intensity of infection on condition (as measured by scaled mass index, plasma metabolites, and feather corticosterone), spring migration departure dates, or home range sizes. We also tested a prediction of the Hamilton–Zuk hypothesis and found that male ornament (song) quality was unrelated to parasitic infection status. Overall, our results provide the first evidence that long‐distance migrants captured on their wintering grounds are in the chronic stage of infection, and suggest that winter studies may fare no better than breeding studies at determining the costs of acute malarial infection for great reed warblers.

MHC, parasites and antler development in red deer: no support for the Hamilton & Zuk hypothesis.

The Hamilton-Zuk hypothesis proposes that the genetic benefits of preferences for elaborated secondary sexual traits have their origins in the arms race between hosts and parasites, which maintains genetic variance in parasite resistance. Infection, in turn, can be reflected in the expression of costly sexual ornaments. However, the link between immune genes, infection and the expression of secondary sexual traits has rarely been investigated. Here, we explored whether the presence and identity of functional variants (supertypes) of the highly polymorphic major histocompatibility complex (MHC), which is responsible for the recognition of parasites, predict the load of lung and gut parasites and antler development in the red deer (Cervus elaphus). While we found MHC supertypes to be associated with infection by a number of parasite species, including debilitating lung nematodes, we did not find support for the Hamilton-Zuk hypothesis. On the contrary, we found that lung nematode load was positively associated with antler development. We also found that the supertypes that were associated with resistance to certain parasites at the same time cause susceptibility to others. Such trade-offs may undermine the potential genetic benefits of mate choice for resistant partners.

Testing the Hamilton-Zuk hypothesis: past, present, and future.

Hamilton and Zuk proposed a good-genes model of sexual selection in which genetic variation can be maintained when females prefer ornaments that indicate resistance to parasites. When trait expression depends on a male's resistance, the co-adaptive cycles between host resistance and parasite virulence provide a mechanism in which genetic variation for fitness is continually renewed. The model made predictions at both the intraspecific and interspecific levels. In the three decades since its publication, these predictions have been theoretically examined in models of varying complexity, and empirically tested across many vertebrate and invertebrate taxa. Despite such prolonged interest, however, it has turned out to be extremely difficult to empirically demonstrate the process described, in part because we have not been able to test the underlying mechanisms that would unequivocally identify how parasites act as mediators of sexual selection. Here, we discuss how the use of high-throughput sequencing datasets available from modern genomic approaches might improve our ability to test this model. We expect that important contributions will come through the ability to identify and quantify the suite of parasites likely to influence the evolution of hosts' resistance, to confidently reconstruct phylogenies of both host and parasite taxa, and, perhaps most exciting, to detect generational cycles of heritable variants in populations of hosts and parasites. Integrative approaches, building on systems undergoing parasite-mediated selection with genomic resources already available, will be particularly useful in moving toward robust tests of this hypothesis. We finish by presenting case studies of well-studied host-parasite relationships that represent promising avenues for future research.

Negative correlation between nuptial throat colour and blood parasite load in male European green lizards supports the Hamilton–Zuk hypothesis

During female mate choice, conspicuous male sexual signals are used to infer male quality and choose the best sire for the offspring. The theory of parasite-mediated sexual selection (Hamilton-Zuk hypothesis) presumes that parasite infection can influence the elaboration of sexual signals: resistant individuals can invest more energy into signal expression and thus advertise their individual quality through signal intensity. By preferring these males, females can provide resistance genes for their offspring. Previous research showed that nuptial throat colour of male European green lizard, Lacerta viridis, plays a role in both inter- and intrasexual selections as a condition-dependent multiple signalling system. The aim of this study was to test the predictions of the Hamilton-Zuk hypothesis on male European green lizards. By blood sampling 30 adult males during the reproductive season, we found members of the Haemogregarinidae family in all but one individual (prevalence = 96%). The infection intensity showed strong negative correlation with the throat and belly colour brightness in line with the predictions of the Hamilton-Zuk hypothesis. In addition, we found other correlations between infection intensity and other fitness-related traits, suggesting that parasite load has a remarkable effect on individual fitness. This study shows that throat patch colour of the European green lizards not only is a multiple signalling system but also possibly acts as an honest sexual signal of health state in accordance with the Hamilton-Zuk hypothesis.

Are large wattles related to particular MHC genotypes in the male pheasant?

In sexually dimorphic species, partners can assess heritable mate quality by analyzing costly sexual ornaments in terms of their dimension and possibly of their symmetry. In vertebrates an important aspect of genetic quality is the efficiency of the immune system, and in particular the Major Histocompatibility Complex (MHC). If ornaments are honest advertisements of pathogen resistance (good genes), in line with the Hamilton-Zuk hypothesis, a correlation between ornament expression and MHC profiles should exist. We tested this hypothesis in the common pheasant Phasianus colchicus by comparing male ornament characteristics (wattle and spur size, and wattle fluctuating asymmetry) with a portion of exon 2 of the class IIB MHC genes containing 19 putative antigen recognition sites. A total of 8 new alleles was observed in the MHCPhco exon IIB. We found significant differences in the occurrence of MHC genotypes between males carrying large or small wattles. Homozygous genotypes predicted large wattle males more correctly than small wattle males. The association between the dimension of the spur and the occurrence of MHC genotypes was marginally significant, however, we did not find any significant association between MHC genotypes and asymmetry. Our results suggest that female pheasants may use the ornament size as a cue to evaluate male quality and thus choose males carrying particular MHC profiles.

Is Brightest Best? Testing the Hamilton-Zuk Hypothesis in Mandrills

Although many primates exhibit striking coloration, including brightly colored pelage and bare areas of skin, our understanding of the function and evolution of these traits pales in the face of knowledge about color in other taxa. However, recent years have seen an increase in the number of studies of individual variation in primate color and evidence is accumulating that these traits can act as important signals to conspecifics. Mandrills are arguably the most colorful of all primates. Here, we review what we have discovered about the signal function of coloration in male and female mandrills from our long-term studies of a semi-free-ranging colony in Franceville, Gabon and test the predictions of the Hamilton-Zuk hypothesis—that bright coloration is condition dependent, and that only individuals of superior quality will be able to express color fully—in this species. We compare measures of facial coloration in both sexes with parasite load (using fecal analysis over 1 annual cycle), immune status (hematological parameters), neutral genetic diversity (microsatellite heterozygosity), and major histocompatability (MHC) genotype to examine whether red coloration acts as an honest signal of individual quality in mandrills. We found that red coloration was unrelated to parasitism and hematological parameters. Red was also unrelated to genome-wide heterozygosity and MHC diversity, although specific MHC genotypes were significantly related to red. The healthy, provisioned nature of the colony and problems associated with observational, correlational studies restrict interpretation of our data, and it would be premature to draw conclusions as to whether color signals individual quality in mandrills. We conclude with some suggestions for future studies on the signal content of color in mandrills and other primates.

Evaluating the Effects of Enteric Helminths on Epigamic Characters of Male Wild Turkeys (Meleagris gallopavo) in Southeastern Kansas, U.S.A.

Costs associated with the production of epigamic characters might make them honest indicators of a male's fitness. The Hamilton–Zuk hypothesis suggests epigamic characters might be indicators of a male's heritable resistance to parasites, predicting a negative correlation between parasite abundance and the elaboration of epigamic characters. Principal component analysis (PCA) of the epigamic characters of 35 male wild turkeys from a zone of Rio Grande (Meleagris gallopavo intermedia) and Eastern (Meleagris gallopavo silvestris) subspecies hybridization revealed variation in characters that covaried with body size (beard length and spur size) and characters that varied independent of body size (snood length and skullcap width), which have the potential for indicating heritable resistance. None of the PCA axes was correlated with mean enteric helminth abundances, suggesting that helminth parasites are not affecting the vigor of male wild turkeys in southeastern Kansas, U.S.A., and apparently, have not exerted selective pressure in the recent past to advertise resistance.

The rise of non-adaptive intelligence in humans under pathogen pressure

Cleverness made our species the most successful primate on Earth, thus claiming that human intelligence is adaptive sounds to be a triviality. Not surprisingly, when establishing long-lasting pair-bonds, humans exhibit mate preferences in favour of clever partners, apparently to increase the chance that their offspring will be as clever as possible. Contrary to this well-established view, here I argue that the adaptive nature of human intelligence has never been proven in a strict evolutionary sense. Furthermore, the exceptional rise of intelligence in our species (and the lack of comparable phenomena in other apes) is best explained within the context of the Hamilton-Zuk Hypothesis. Apparently, humans have been subjected to an exceptionally strong selection pressure exerted by pathogens and parasites, and the human brain is particularly vulnerable to infections, thus cleverness is an ideal character to signal heritable genetic resistance against infections. In this scenario, human preference for intelligent mates is to increase the offspring's resistance against pathogens. Among other phenomena, this hypothesis can explain why humans enjoy wasting most of their intellectual capabilities for totally useless purposes, why prehistoric humans developed brains that made them potentially far more intelligent than required by their physical environment, and why we experience a continuous increase of human intelligence even in modern societies. Briefly, I argue that (1) human sexual selection favours intelligence as a signal of genetic resistance against pathogens, and (2) that intelligence enabled the rise of our species (in terms of population size and distribution) as an accidental side-effect.

A field test of the Hamilton–Zuk hypothesis in the Trinidadian guppy (Poecilia reticulata)

The Hamilton–Zuk hypothesis proposes that females prefer male secondary sexual traits because they are honest indicators of parasite resistance. Despite the attention that this hypothesis has received, its role in sexual selection remains equivocal. This study presents the first field test in guppies of two key predictions of the Hamilton–Zuk hypothesis: (1) that within populations, the most highly ornamented males have the fewest parasites and (2) that among populations, males in high parasite populations have the most conspicuous ornaments. Five hundred male guppies from 19 distinct populations in the Northern Range of Trinidad were inspected for Gyrodactylus parasites and photographed. Eight measures of orange spot ornamentation were used to test the predictions: hue, saturation, lightness, relative area, number, and area-weighted hue, saturation, and lightness. Parasite load had no significant effect on any of these measures. There was also no relationship between orange spot ornamentation and parasite abundance among populations. Guppies from high-predation environments had significantly more parasites, and their orange coloration was lighter and less saturated than that in guppies from low-predation environments. Despite previous lab results, this study found no relationship between parasite load and male orange spot ornamentation.

Parasites affect song complexity and neural development in a songbird

There is now considerable evidence that female choice drives the evolution of song complexity in many songbird species. However, the underlying basis for such choice remains controversial. The developmental stress hypothesis suggests that early developmental conditions can mediate adult song complexity by perturbing investment in the underlying brain nuclei during their initial growth. Here, we show that adult male canaries (Serinus canaria), infected with malaria (Plasmodium relictum) as juveniles, develop simpler songs as adults compared to uninfected individuals, and exhibit reduced development of the high vocal centre (HVC) song nucleus in the brain. Our results show how developmental stress not only affects the expression of a sexually selected male trait, but also the structure of the underlying song control pathway in the brain, providing a direct link between brain and behaviour. This novel experimental evidence tests both proximate and ultimate reasons for the evolution of complex songs and supports the Hamilton-Zuk hypothesis of parasite-mediated sexual selection. Together, these results propose how developmental costs may help to explain the evolution of honest advertising in the complex songs of birds.

Carotenoid-based plumage coloration predicts resistance to a novel parasite in the house finch

The Hamilton-Zuk hypothesis proposes that the bright colours displayed by many species of birds serve as signals of individual resistance to parasites. Despite the popularity of this hypothesis, only one previous study has tested whether plumage coloration predicts how individuals respond to a disease challenge. We inoculated 24 male house finches (Carpodacus mexicanus) of variable plumage hue with a novel bacterial pathogen, Mycoplasma gallicepticum (MG). We found no relationship between plumage hue and time to first symptoms following inoculation, but we found a significant negative relationship between plumage hue and clearance of disease: males with redder plumage cleared MG infection significantly better than did males with yellower plumage. The hue of carotenoid-based plumage coloration has been shown to be a primary criterion in female mate choice in the house finch. These observations suggest that one benefit to females for choosing redder males is obtaining mates with better resistance to parasites.

Do blood parasites affect reproductive performance in male red bishops (Euplectes orix)? A test of the Hamilton-Zuk hypothesis

According to the Hamilton-Zuk hypothesis of parasite-mediated sexual selection the expression of male secondary sexual characters as well as health and condition should be negatively affected by parasites. Over five breeding seasons we investigated the relationship between prevalence and intensity of blood parasites and reproductive performance as well as health state in male red bishops (Euplectes orix), a highly polygynous weaverbird species common in southern Africa. Neither prevalence nor intensity of infections with Plasmodium sp., the only blood parasite found in this study, were related to two important measures of male reproductive performance, i.e. the number of nests built (an intrasexually selected trait which is the most important determinant of male mating success) and the ability to establish a territory. In addition, parasite prevalence and intensity were not affected by season, time within season, age or body condition. These results do not support predictions derived from the Hamilton-Zuk hypothesis of parasite-mediated sexual selection. However, our data indicate that high stress levels as assessed by the heterophile/lymphocyte ratio might increase parasite susceptibility.