Matthew R. Evans

Testing the immunocompetence handicap hypothesis: a review of the evidence

The immunocompetence handicap hypothesis was formulated 12 years ago in an attempt to offer a proximate mechanism by which female choice of males could be explained by endocrine control of honest signalling. The hypothesis suggested that testosterone has a dual effect in males of controlling the development of sexual signals while causing immunosuppression. Our purpose in this review is to examine the empirical evidence to date that has attempted to test the hypothesis, and to conduct a meta-analysis on two of the assumptions of the hypothesis, that testosterone reduces immunocompetence and increases parasitism, to ascertain any statistical trend in the data. There is some evidence to suggest that testosterone is responsible for the magnitude of trait expression or development of sexual traits, but this is by no means conclusive. The results of many studies attempting to find evidence for the supposed immunosuppressive qualities of testosterone are difficult to interpret since they are observational rather than experimental. Of the experimental studies, the data obtained are ambiguous, and this is reflected in the result of the meta-analysis. Overall, the meta-analysis found a significant suppressive effect of testosterone on immunity, in support of the hypothesis, but this effect disappeared when we controlled for multiple studies on the same species. There was no effect of testosterone on direct measures of immunity, but it did increase ectoparasite abundance in several studies, in particular in reptiles. A funnel analysis indicated that the results were robust to a publication bias. Alternative substances that interact with testosterone, such as glucocorticoids, may be important. Ultimately, a greater understanding is required of the complex relationships that exist both within and between the endocrine and immune systems and their consequences for mate choice decision making.

The effects of testosterone on antibody production and plumage coloration in male house sparrows (Passer domesticus)

Abstract Many bird species have patches of colour in their plumage, contrasting with their basic coloration, which are used to display and signal status to conspecifics. These are called ’badges of status’, because they are believed to be low-cost signals of social status. For a signalling system to be evolutionarily stable, cheating must be controlled. The conventional view is that there is frequent testing, which uncovers cheats. Recently, the immunocompetence handicap hypothesis (ICHH) suggested that signals may be dependent on testosterone for their development, with a cost being imposed through immune suppression. We report experiments on house sparrows (Passer domesticus) which show that testosterone significantly influences the size of the bib (a ’badge of status’). The ultimate effect of the testosterone manipulation was to impair antibody production, as predicted by the ICHH. However, testosterone manipulations also changed the levels of the ’stress hormone’ corticosterone. The level of corticosterone was also related to the degree of immunosuppression. After controlling for the effect of corticosterone, testosterone enhanced the birds’ ability to produce antibodies, counter to the ICHH. The hypothesis therefore must be modified. We suggest that testosterone has a dual effect: it leads to immunosuppression through a mechanism involving corticosterone but, conversely, leads to increased immunocompetence probably via dominance influencing access to resources.

Testosterone influences basal metabolic rate in male house sparrows: a new cost of dominance signalling?

Sexually selected signals of individual dominance have profound effects on access to resources, mate choice and gene flow. However, why such signals should honestly reflect individual quality is poorly understood. Many such signals are known to develop under the influence of testosterone. We conducted an experiment in male house sparrows in which testosterone was manipulated independently during two periods: before the onset of the breeding season and prior to the autumn moult. We then measured the effects of these manipulations on basal metabolic rate and on the size of the chest bib, a sexually selected signal. The results demonstrate that testosterone simultaneously affects both signal development and basal metabolic rate in the house sparrow (Passer domesticus). This evidence, therefore, supports a novel conclusion: that testosterone–dependent signals act as honest indicators of male quality possibly because only high–quality individuals can sustain the energetic costs associated with signal development.

Heritability of corticosterone response and changes in life history traits during selection in the zebra finch

Vertebrates respond to environmental stressors through the neuro‐endocrine stress response, which involves the production of glucocorticoids. We have selected independent, duplicate divergent lines of zebra finches for high, low and control corticosterone responses to a mild stressor. This experiment has shown that over the first four generations, the high lines have demonstrated a significant realized heritability of about 20%. However, the low lines have apparently not changed significantly from controls. This asymmetry in response is potentially because of the fact that all birds appear to be showing increased adaptation to the environment in which they are housed, with significant declines in corticosterone response in control lines as well as low lines. Despite the existence of two‐ to threefold difference in mean corticosterone titre between high and low lines, there were no observed differences in testosterone titre in adult male birds from the different groups. In addition, there were no consistent, significant differences between the lines in any of the life history variables measured – number of eggs laid per clutch, number of clutches or broods produced per pair, number of fledglings produced per breeding attempt, nor in any of egg, nestling and fledgling mortality. These results highlight the fact that the mechanisms that underlie variation in the avian physiological system can be modified to respond to differences between environments through selection. This adds an additional level of flexibility to the avian physiological system, which will allow it to respond to environmental circumstances.

Testosterone, dominance signalling and immunosuppression in the house sparrow, Passer domesticus

The immunocompetence handicap hypothesis (ICHH) suggests that dominance signals are costly because their development is controlled by testosterone, which is immunosuppressive. Signal control therefore links an increased disease risk with a high quality signal. The chest bib of the house sparrow, Passer domesticus, is a signal known to be related to dominance and under control of testosterone levels. We experimentally manipulated testosterone in male sparrows during the breeding season and again independently during the post-breeding period to test whether variation in levels of testosterone could cause variation in levels of immunocompetence. There was no effect of testosterone manipulation on the cell-mediated response of birds to phytohaemagglutinin injection, nor did testosterone levels appear to affect either white blood cell ratios or red blood cell counts. In contrast, both breeding season and post-breeding season testosterone levels had significant effects upon the humoral response of the birds to sheep red blood cell injections. However, whilst testosterone during the breeding season appeared to act immunosuppressively, the role of post-breeding levels is less clear. In concordance with a previous study, there was an indication that corticosterone is involved in mediating the immunosuppressive effects of testosterone. The strength of the secondary humoral response and the cell-mediated response were negatively related suggesting the possibility of a trade-off between the different arms of the immune system. These results provide some support for the ICHH as a mechanism promoting the evolution of costly badges of status, although the results question whether the immunosuppressive cost can be mediated by testosterone at the time of badge development.

An experimental study of male adornment in the scarlet-tufted malachite sunbird: II. The role of the elongated tail in mate choice and experimental evidence for a handicap

SummaryScarlet-tufted malachite sunbirds (Neetarinia johnstoni) are endemic to the high altitude zones of East African mountains. On Mount Kenya the males are resident and territorial all year. The females arrive over an extended period at the beginning of the breeding season, after spending the non-breeding season in nomadic flocks at slightly lower elevations. Males are bright iridescent green with elongated central tail feathers, which are displayed during courtship. We examined the role of the tail in mate choice using natural variation and investigated the influence of tail length on male time budgets by experimental manipulation. Territorial males that paired had longer tails than territorial males which remained unpaired. Males with naturally long tails started breeding earlier, resulting in fledglings being produced earlier in the season when the weather was more clement. Birds which bred together in one year were paired together in the next year if they both survived. Thus the males tail may only be involved as a cue in the formation of new pairs. Males which were already paired were subjected to one of three experimental treatments — having their tail elongated, shortened, or manipulated but kept at the same length. Males with experimentally shortened tails spent more time in flight and hawked for flying insects with a higher efficiency than control males. Both control and elongated tail males reduced the amount of time in flight and had a lower hawking efficiency after manipulation. These results suggest that the long tail of male scarlet-tufted malachite sunbirds is a handicap. The factors influencing the reproductive success of a pair are discussed.

Ectoparasites of house sparrows (Passer domesticus): an experimental test of the immunocompetence handicap hypothesis and a new model

Abstract Conspicuous secondary sexual traits may have evolved as handicap-revealing signals or as badges of status. We present results of an experiment using males of the sexually dimorphic house sparrow (Passer domesticus), that support the idea that the male-specific bib can be both a handicap-revealing signal and a reliable badge indicating the physical condition of the bird. In a test of the immunocompetence handicap hypothesis, wild-caught adult male house sparrows were studied in captivity. Birds implanted with elevated doses of testosterone were more dominant, had higher circulating levels of both testosterone and corticosterone and they also harboured relatively larger ectoparasite loads. Higher parasite loads were also associated with individuals showing lower immunocompetence and larger changes in bib size. A new model for immunocompetence effects in sexual selection is introduced, integrating actions that the hypothalamopituitary axis exerts on gonads, adrenals and the thyroid gland. The ”integrated immunocompetence model” synthesizes both the ”handicap” (i.e. survival-decreasing) and ”badge of status” (i.e. survival- enhancing) models for evolution of secondary sexual traits.

Effects of testosterone and corticosterone on immunocompetence in the zebra finch.

The original immunocompetence handicap hypothesis (ICHH) suggested that testosterone has a handicapping effect in males by both promoting the development of sexual signals and suppressing immune function. A modified version, the stress-linked ICHH, has recently proposed that testosterone is immunosuppressive indirectly by increasing production of corticosterone. To test both the original and stress-mediated versions of the ICHH, we implanted male zebra finches taken from lines selected for divergent maximum stress-induced levels of corticosterone (high, low and control) with either empty or testosterone-filled implants. Their humoral and cell-mediated immune responses were then assessed by challenge with diphtheria:tetanus vaccine and phytohemagglutinin respectively. We found no effect of the hormone manipulations on either PHA or tetanus antibody responses, but found a significant interaction between titers of both testosterone and corticosterone on diphtheria secondary antibody response; antibody response was greatest in individuals with high levels of both hormones. There was also a significant interactive effect between testosterone treatment group and corticosterone titer on body mass; the body mass of males in the elevated testosterone treatment group decreased with increasing corticosterone titer. These results suggest that, contrary to the assumption of the stress-mediated version of the ICHH, high plasma levels of corticosterone are not immunosuppressive, but are in fact immuno-enhancing in the presence of high levels of plasma testosterone. Equally, the central assumption of the ICHH that testosterone is obligately immunosuppressive is also not supported. The same individuals with the highest levels of both hormones and consequently the most robust antibody response also possessed the lowest body mass.

An experimental study of male adornment in the scarlet-tufted malachite sunbird: I. The role of pectoral tufts in territorial defence

SummaryScarlet-tufted malachite sunbirds (Nectarinia johnstoni) are endemic to the alpine zones of East African mountains. On Mount Kenya they feed almost exclusively on the nectar of Lobelia telekii flowers. Males are resident on their territories all year and defend L. telekii inflorescences from conspecifics. Males are bright iridescent green, with scarlet pectoral tufts which are displayed prominently during aggressive interactions with other males. We investigated the role of pectoral tufts in territory defence using natural variation and experimental manipulation. Males with naturally large pectoral tufts defended more L. telekii inflorescences than males with smaller tufts, and achieved a higher reproductive success. Males were subjected to one of three experimental treatments - having their pectoral tufts enlarged, reduced or manipulated but kept at the same size. Males with reduced tufts spend more time in aggressive interactions than the control males, the interactions lasted longer and they lost a number of inflorescences to neighbours. Males with enlarged pectoral tufts increased the number of inflorescences defended. These results indicate that the pectoral tufts of male scarlet-tufted malachite sunbirds are used as a means of male-male assessment during aggressive interactions.

The House Sparrow Passer domesticus in urban areas: reviewing a possible link between post-decline distribution and human socioeconomic status

The House Sparrow Passer domesticus is traditionally associated with human habitation. However, the species has undergone dramatic declines in many urban areas in north-western Europe. There are many theories as to why this decline has occurred, but the lack of data on House Sparrow numbers prior to their decline has hampered efforts to investigate these theories in detail. This review summarises the demographic changes in urban House Sparrow populations since the 1970s, and considers evidence that the current distribution of House Sparrows may reflect changes in urban habitats caused by socioeconomic change. Evidence is mounting that, within urban landscapes, House Sparrows appear to be more prevalent in areas with a relatively low human socioeconomic status. Here, we present evidence to suggest that House Sparrows may have disappeared predominantly from more affluent areas, and that these areas are more likely to have undergone changes to habitat structure. We also show how these changes in habitat could influence House Sparrow populations via impacts upon nesting success, foraging and predation risk.