Microhabitat selection and audible sexual signalling in the wolf spider Hygrolycosa rubrofasciata (Araneae, Lycosidae)

We studied the microhabitat selection and male sexual signalling behaviour in the wolf spider Hygrolycosa rubrofasciata (Ohlert). Males strike dry leaves with their abdomen, producing an audible sexual drumming signal, and females use this signal to choose mating partners. In the field we followed male drumming rate and microhabitat selection using both the mark–recapture method and direct observations. In the laboratory we conducted an experiment on male microhabitat and drumming substrate selection. We found that in the field males were not distributed randomly among the habitat; fewer males were found in areas that had high sedge cover, low elevation, and low dry leaf cover. In the laboratory experiment, males spent more time on dry leaf substrate. Drumming rate in the field was positively correlated with dry leaf cover and in the laboratory males clearly preferred dry leaves as drumming substrate. Temperature was positively correlated with male drumming rate, and with male and female mobility. We conclude that in H. rubrofasciata male distribution and sexual signalling rate, and thus mating success, are greatly affected by environmental factors. Therefore, males may be sexually selected to make effective use of their signalling habitat by active microhabitat choice. Received: 27 December 1999 / Received in revised form: 14 February 2000 / Accepted: 14 February 2000     

Sexual selection in the wolf spider Hygrolycosa rubrofasciata: female preference for drum duration and pulse rate

The unusual form of sexual signaling, the drumming producedby the wolf spider Hygrolycosa rubrofasciata, allows exceptionallydetailed studies of female preference patterns against signalcharacteristics. It is easy to manipulate the signals and touse large numbers of females in playback experiments. Malesof H. rubrofasciata produce drums by striking their abdomenagainst dry leaves on the ground. Drums travel not only as substrate-borne vibrations, but also as airborne acoustic signals.Females respond sooner to drums transferred as substrate borne,but the mode of signal transfer has no effect on female preferencefor different types of drums. We investigated the effects oftwo key components of the drums, duration and pulse rate, onfemale choice. Previous studies have shown that the durationof the drum is both repeatable within males and variable betweenmales. In contrast, pulse rate shows high within-male repeatabilitybut only little variability between males. Using playbacksof manipulated drums, we found that females preferred drumsof longer duration but that pulse rate had no effect on femalepreference. Our results suggest that drum duration may functionas an indicator of male quality for choosy females. Pulse rate,on the other hand, is less likely to be an important traitin intersexual selection. Female preference for drum durationwas open-ended within the natural variation of the drum durations,but it leveled off outside the normal range. Thus supernomalstimuli would not pay for males using this energetically demanding acoustic signal.     

Courtship song and immune function in the field cricket Gryllus bimaculatus

It has been assumed that sexual ornaments have evolved to reveal males' health and vigour for females. Choosy females may indirectly use ornaments as an indicator of the presence and effectiveness of genes for resistance against parasites. In this study we tested whether females of the Mediterranean field cricket, Gryllus bimaculatus, can use courtship song as a cue for choosing males with high immunocompetence, measured as encapsulation rate of nylon implants and lytic activity of haemolymph. We found that female crickets preferred courtship songs from males with a high encapsulation rate. Female crickets also had a tendency to prefer courtship songs with high tick rate and long high-frequency tick duration. These preferred song components were positively correlated with encapsulation rate, but negatively correlated with lytic activity of the male. In contrast to previous studies of crickets, there was no correlation between male weight and encapsulation rate or lytic activity. There is some evidence in another cricket species that the ability to encapsulate pathogens is heritable. Thus, in light of this study it seems possible that by preferring males according to their courtship song, females might benefit by increasing the parasite resistance of their offspring.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79 , 503–510.     

Host immune function and sexual selection in birds

Parasites have been hypothesized to affect sexual selection of their hosts, if secondary sexual characters reliably signal absence of infectious parasites, superior parenting ability caused by the absence of parasites, or heritable resistance to parasites, for which there is some intraspecific and interspecific evidence. Measures of immune defence of hosts provide reliable information on the current infection status of individuals of the chosen sex, usually males, and correlations between immune defence and development of secondary sexual characters thus provide a novel critical test of parasite-mediated sexual selection. In a comparative study of birds, sexually dichromatic species had higher immune defences, measured in terms of leukocyte concentration and the size of spleen and bursa of Fabricius, respectively, than closely related, monochromatic species. Male plumage brightness was consistently negatively related to the size of the spleen in males of sexually dichromatic species, but not in males of monochromatic species. Hence, the brightest males, which frequently are preferred as mates by choosy females, had low levels of immune defence, suggesting that such males were healthy. This provides evidence for a general role of parasites in sexual selection among their bird hosts.     

Forceps size and immune function in the earwig Forficula auricularia L.

Females of many species select their mates on the basis of the size or intensity of sexual ornaments, and it has been suggested that these provide reliable signals of a male's ability to resist parasites and pathogens. European earwigs, Forficula auricularia , are sexually dimorphic in forceps shape and length. Male forceps are used as weapons in male contests for access to females, but recent findings suggest that females also choose males on the basis of their forceps length. In the present study, we tested the hypotheses that in the European earwig, F. auricularia , the size of forceps is correlated with immune function and that immune function differs between the sexes. We found that encapsulation rate was not correlated with the length of forceps in either sex, but was negatively correlated with body size. By contrast, lytic activity of the haemolymph increased with overall body size in both sexes but, in females, lytic activity increased with relative forceps length whereas, in males, it decreased with relative forceps length. After accounting for effects of body size, there was no remaining significant correlation in females but the negative correlation in males remained. Furthermore, we found that males had higher encapsulation rate and higher lytic activity than females, suggesting that males have stronger immune defence. The results of the study indicate that the size of forceps in male earwigs does not reliably reflect male immune defence.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 509–516.     

Male morph predicts investment in larval immune function in the dung beetle, Onthophagus taurus

Investment in immunity is costly, so that resource-based trade-offsbetween immunity and sexually selected ornaments might be expected.The amount of resources that an individual can invest in eachtrait will be limited by the total resources available to them.It would therefore be informative to investigate how investmentin immune function changes during growth or production of thesexual trait as resources are diverted to it. Using the dungbeetle, Onthophagus taurus, which displays both sexual and maledimorphism in horn size, we examined changes in one measureof immune function, phenoloxidase (PO) activity, in the hemolymphof larvae prior to and during horn growth. We found that POlevels differed between small- and large-horned males throughoutthe final instar prior to the point where investment in horngrowth was taking place. PO levels in females were intermediateto the 2 male morphs. These differences could not be accountedfor by differences in condition, measured as hemolymph proteinlevels and weight. We suggest that the observed differencesmight be associated with sex- and morph-specific variation injuvenile hormone levels.     

A trade-off between sexual signalling and immune function in a natural population of the drumming wolf spider Hygrolycosa rubrofasciata

The field of ecological immunology is ultimately seeking to address the question ‘Why is there variation in immune function?’ Here, we provide experimental evidence that costs of ubiquitous sexual signals are a significant source of variation in immune function. In the mating season, males of the wolf spider Hygrolycosa rubrofasciata drum against dry leaves while wandering around the habitat searching for receptive females. According to a previous study, the male metabolic rate during the drumming increases 22‐fold compared to the resting metabolic rate. In the present study, we examined whether investment in costly courtship drumming decreases male immune function in a wild population of H. rubrofasciata. We induced males to increase their drumming rate by introducing females in proximity. As estimates of male immune function, we used lytic activity and encapsulation rate. Lytic activity estimates the concentration of antimicrobial peptides in haemolymph, which have been shown to play an important role in defence against bacteria, viruses and fungi. Encapsulation is an important defence mechanism against nematodes and insect parasitoids, but it also plays a role in defence against viruses. Our results show that males with nonarbitrarily increased investment in drumming rate had considerably lower lytic activities than control males. Also, there was a tendency for males with nonarbitrarily increased investment in drumming rate to have lower encapsulation rates than control males. This study provides experimental evidence for the first time, to our knowledge, that there are direct immunological costs of sexual signalling in natural populations. Therefore, immunological costs of sexual signals may provide significant phenotypic variation to parasite‐mediated sexual selection.     

Sexual selection and immune function in Drosophila melanogaster

The evolution of immune function depends not only on variation in genes contributing directly to the immune response, but also on genetic variation in other traits indirectly affecting immunocompetence. In particular, sexual selection is predicted to trade-off with immunocompetence because the extra investment of resources needed to increase sexual competitiveness reduces investment in immune function. Additional possible immunological consequences of intensifying sexual selection include an exaggeration of immunological sexual dimorphism, and the reduction of condition-dependent immunological costs due to selection of 'good genes' (the immunocompetence handicap hypothesis, ICHH). We tested for these evolutionary possibilities by increasing sexual selection in laboratory populations of Drosophila melanogaster for 58 generations by reestablishing a male-biased sex ratio at the start of each generation. Sexually selected flies were larger, took longer to develop, and the males were more sexually competitive than males from control (equal sex ratio) lines. We found support for the trade-off hypothesis: sexually selected males were found to have reduced immune function compared to control males. However, we found no evidence that sexual selection promoted immunological sexual dimorphism because females showed a similar reduction in immune function. We found no evidence of evolutionary changes in the condition-dependent expression of immunocompetence contrary to the expectations of the ICHH. Lastly, we compared males from the unselected base population that were either successful (IS) or unsuccessful (IU) in a competitive mating experiment. IS males showed reduced immune function relative to IU males, suggesting that patterns of phenotypic correlation largely mirror patterns of genetic correlation revealed by the selection experiment. Our results suggest increased disease susceptibility could be an important cost limiting increases in sexual competitiveness in populations experiencing intense sexual selection. Such costs may be particularly important given the high intersex correlation, because this represents an apparent genetic conflict, preventing males from reaching their sexually selected optimum.     

Inter- and intra-sexual variation in immune defence in the cabbage white butterfly, Pieris rapae L. (Lepidoptera: Pieridae)

Abstract.  1. Immune defence imposes fitness costs as well as benefits, so organisms are expected to optimise, not maximise, their immune responses. This should result in variation in immune responses under varying environmental conditions.
2. Males and females are expected to exhibit different immune responses because life-history differences between the sexes affect optimal immune response. These life-history differences should usually result in a greater female, than male, immune defence. In this study, intra- and inter-sexual variation in one component of immune defence, the encapsulation response, in cabbage white butterflies ( Pieris rapae L.), was examined.
3. Encapsulation decreased with increasing age and in response to reduced diet quality.
4. Contrary to predictions, males generally had greater immune responses than females, although this pattern varied with age.
5. These patterns of inter- and intra-sexual variation in encapsulation may result from resource-based trade-offs with components of reproductive effort and/or because of sexual dimorphism in melanin-based wing patterns.     

Sexual conflict and the function of genitalic claws in guppies (Poecilia reticulata)

Poeciliid fish, freshwater fish with internal fertilization, are known for the diversity of structures on the male intromittent organ, the gonopodium. Prominent among these, in some species, is a pair of claws at its tip. We conducted a manipulative study of these claws in the guppy, Poecilia reticulata, to determine if these aid in transferring sperm to resistant females. We compared the sperm transfer rates of clawed versus surgically declawed males attempting to mate with either receptive or unreceptive (i.e. resistant) females. Our analyses demonstrate that the gonopodial claws function to increase sperm transfer to unreceptive females during uncooperative matings but not during receptive matings. Up to threefold more sperm were transferred to unreceptive females by clawed than declawed males. These data suggest that the claw is a sexually antagonistic trait, functioning to aid in transferring sperm to resistant females, and implicate sexual conflict as a selective force in the diversification of the gonopodium in the Poeciliidae.     

The effects of sex hormones on immune function: a meta‐analysis

The effects of sex hormones on immune function have received much attention, especially following the proposal of the immunocompetence handicap hypothesis. Many studies, both experimental and correlational, have been conducted to test the relationship between immune function and the sex hormones testosterone in males and oestrogen in females. However, the results are mixed. We conducted four cross‐species meta‐analyses to investigate the relationship between sex hormones and immune function: (i) the effect of testosterone manipulation on immune function in males, (ii) the correlation between circulating testosterone level and immune function in males, (iii) the effect of oestrogen manipulation on immune function in females, and (iv) the correlation between circulating oestrogen level and immune function in females. The results from the experimental studies showed that testosterone had a medium‐sized immunosuppressive effect on immune function. The effect of oestrogen, on the other hand, depended on the immune measure used. Oestrogen suppressed cell‐mediated immune function while reducing parasite loads. The overall correlation (meta‐analytic relationship) between circulating sex hormone level and immune function was not statistically significant for either testosterone or oestrogen despite the power of meta‐analysis. These results suggest that correlational studies have limited value for testing the effects of sex hormones on immune function. We found little evidence of publication bias in the four data sets using indirect tests. There was a weak and positive relationship between year of publication and effect size for experimental studies of testosterone that became non‐significant after we controlled for castration and immune measure, suggesting that the temporal trend was due to changes in these moderators over time. Graphical analyses suggest that the temporal trend was due to an increased use of cytokine measures across time. We found substantial heterogeneity in effect sizes, except in correlational studies of testosterone, even after we accounted for the relevant random and fixed factors. In conclusion, our results provide good evidence that testosterone suppresses immune function and that the effect of oestrogen varies depending on the immune measure used.     

Evidence for the signaling function of egg color in the pied flycatcher Ficedula hypoleuca

A recent hypothesis proposes that the bright colors, especiallyblue and green, of many avian eggs may function as signals offemale or offspring phenotypic quality or condition to malesin species with biparental care, inducing them to allocate moreeffort to their offspring. The pigment determining blue andgreen egg colors is an antioxidant whose availability for eggshellcoloring may be limited. To test the signaling function on aspecies with blue eggs, the pied flycatcher Ficedula hypoleuca,we measured egg color with a spectrophotometer on the day oflaying and obtained two principal components from their reflectancespectra that together explained 99% of variation and representedshell lightness, and hue and saturation, respectively. We alsomeasured female immunocompetence during the nestling periodthrough the response to phytohemagglutinin as a measure of cell-mediatedimmunity and the response to a tetanus vaccination as a measureof humoral immunity. The total amount of immunoglobulins inblood of females and of nestlings before fledging was also estimated.Mean within-clutch egg darkness was positively associated withboth measures of female immunocompetence, while better femalecondition was associated with colors tending away from intermediateand toward short wavelengths. Ageing female laid lighter eggs.The mean within-brood level of nestling IgY was also associatedwith mean within-clutch egg colors tending away from intermediateand toward short wavelengths. Mean egg darkness decreased linearlyduring the laying sequence, suggesting pigment limitation. Maleswere observed frequently visiting nests during the laying period,allowing them to observe eggs before the start of incubation.These results support the signaling hypothesis for explainingbright colors of avian eggs.     

Sexual behavior in female western lowland gorillas (Gorilla gorilla gorilla): evidence for sexual competition

Previous research in gorillas suggests that females engage in post‐conception mating as a form of sexual competition designed to improve their own reproductive success. This study focused on sexual behaviors in a newly formed group of western lowland gorillas (Gorilla gorilla gorilla) housed at Zoo Atlanta. All females engaged in mating outside their conceptive periods, although there was individual variation in the frequency of the behavior. An analysis of the presence/absence of sexual behavior found females, regardless of reproductive condition, were more likely to engage in sexual behavior on days when other females were sexually active. On these “co‐occurrence” days, females were significantly more likely to solicit the silverback, but copulations did not differ from expectation. The results find further evidence for sexual competition among female gorillas and suggest that this may occur throughout their reproductive cycle rather than only during pregnancy. Am. J. Primatol. 71:587–593, 2009. © 2009 Wiley‐Liss, Inc.     

Sexual reproductive structures of Latest Proterozoic multicellular rhodophytes (red algae) from South China

Carposporangium- and spermatangium-like reproductive structures associated with differentiated vegetative tissues have been observed in the multicellular rhodophyte fossils, which were well preserved in the 650-Ma-old phosphate rocks of Doushantuo Formation in Guizhou Province, South China. The fossils show details of cellular structures that are comparable to the female and male reproductive organs of some extant rhodophytes. The first fossil-histological evidence for sexuality of Precambrian non-vascular plants is provided.     

Humoral immune response in relation to senescence, sex and sexual ornamentation in the barn swallow (Hirundo rustica)

Performance of animals may decline with age. The effects of senescence, however, may differ between the sexes because of differences in physiology and behaviour. Acquired immunity provides hosts with efficient mechanisms of anti-parasite defence, but the effect of senescence on immunocompetence has never been studied in natural populations. In the barn swallow (Hirundo rustica), primary antibody response to an antigen during one breeding season declined with age in females, while secondary response during the following breeding season declined with age in both sexes. Parasite-mediated sexual selection theory posits that male secondary sexual characters reveal resistance to parasites. Males with large tail ornaments had stronger primary response, retained larger antibody levels until the following year, but did not differ in secondary response compared with short-tailed males, as predicted if ornamentation reflects resistance to parasites. This is the first study showing that immunocompetence declines with age in any vertebrate under natural conditions.     

Mate choice, operational sex ratio, and social promiscuity in a wild population of the long-snouted seahorse Hippocampus guttulatus

Mate competition and mate choice are not mutually exclusivebehaviors. Both behaviors may drive sexual selection in oneor both sexes of a population. One of several factors affectingwhich behavior is exhibited by which sex is the operationalsex ratio (OSR) in the study population. The present study combinesbehavioral observations in the field with controlled experimentsin aquaria to investigate social interactions and mate choicein both male and female long-snouted seahorses Hippocampus guttulatusin the context of the population OSR. Compared with the morereadily studied pipefishes, data on OSR and mate choice in seahorsesare scarce in the published literature. Our field data providenovel evidence of social promiscuity, size-assortative mating,and an OSR that varies from being unbiased early and midseasonto male biased at the end of the breeding season. Our mate choiceexperiments revealed intersexual differences in mate preferencewith males significantly preferring larger females to familiarones. Taken together, our field and experimental results suggestthat mate choice rather than intrasexual competition could drivesexual selection in seahorses.     

Scent-marking displays provide honest signals of health and infection

Males of many species produce scent marks and other olfactorysignals that function to intimidate rivals and attract females.It has been suggested that scent marks provide an honest, cheat-proofdisplay of an individual's health and condition. Here we reportseveral findings that address this hypothesis in wild-derivedhouse mice (Mus musculus domesticus). (1) We exposed males tofemale odor, which induces an increase in testosterone, andfound that sexual stimulation significantly increased the males'scent-marking and the attractiveness of their scent marks tofemales. (2) We challenged sexually stimulated males with anonreplicating strain of bacteria (Salmonella enterica C5TS)to activate immunity and found that this significantly decreasedthe males' scent-marking and the attractiveness of their scentmarks to females. (3) We collected scent marks from infectedand sham-infected males when they were sexually stimulated ornot, and we found that females could significantly discriminatethe scent marks of infected versus control males, but only whenthe males were sexually stimulated. Taken together, our resultsindicate that male mice modulate their scent-marking displaydepending on their health and perceived mating opportunities.Increased scent marking enhances males' attractiveness to females,scent marks provide an honest indicator of bacterial infection(and perhaps immune activation), and females are able to assessthe health of males more easily when males mark at a high rate.