Verbal proficiency as fitness indicator: Experimental and comparative research on the evolutionary psychology of language and verbal displays

Summary: Recent research on the evolution of language and verbal displays (e.g., Miller, 1999, 2000a, 2000b, 2002) indicated that language is not only the result of natural selection but serves as a sexually-selected fitness indicator that is an adaptation showing an individual’s suitability as a reproductive mate. Thus, language could be placed within the framework of concepts such as the handicap principle (Zahavi, 1975). There are several reasons for this position: Many linguistic traits are highly heritable (Stromswold, 2001, 2005), while naturally-selected traits are only marginally heritable (Miller, 2000a); men are more prone to verbal displays than women, who in turn judge the displays (Dunbar, 1996; Locke & Bogin, 2006; Lange, in press; Miller, 2000a; Rosenberg & Tunney, 2008); verbal proficiency universally raises especially male status (Brown, 1991); many linguistic features are handicaps (Miller, 2000a) in the Zahavian sense; most literature is produced by men at reproduction-relevant age (Miller, 1999). However, neither an experimental study investigating the causal relation between verbal proficiency and attractiveness, nor a study showing a correlation between markers of literary and mating success existed. In the current studies, it was aimed to fill these gaps. In the first one, I conducted a laboratory experiment. Videos in which an actor and an actress performed verbal self-presentations were the stimuli for counter-sex participants. Content was always alike, but the videos differed on three levels of verbal proficiency. Predictions were, among others, that (1) verbal proficiency increases mate value, but that (2) this applies more to male than to female mate value due to assumed past sex-different selection pressures causing women to be very demanding in mate choice (Trivers, 1972). After running a two-factorial analysis of variance with the variables sex and verbal proficiency as factors, the first hypothesis was supported with high effect size. For the second hypothesis, there was only a trend going in the predicted direction. Furthermore, it became evident that verbal proficiency affects long-term more than short-term mate value. In the second study, verbal proficiency as a menstrual cycle-dependent mate choice criterion was investigated. Basically the same materials as in the former study were used with only marginal changes in the used questionnaire. The hypothesis was that fertile women rate high verbal proficiency in men higher than non-fertile women because of verbal proficiency being a potential indicator of “good genes”. However, no significant result could be obtained in support of the hypothesis in the current study. In the third study, the hypotheses were: (1) most literature is produced by men at reproduction-relevant age. (2) The more works of high literary quality a male writer produces, the more mates and children he has. (3) Lyricists have higher mating success than non-lyric writers because of poetic language being a larger handicap than other forms of language. (4) Writing literature increases a man’s status insofar that his offspring shows a significantly higher male-to-female sex ratio than in the general population, as the Trivers-Willard hypothesis (Trivers & Willard, 1973) applied to literature predicts. In order to test these hypotheses, two famous literary canons were chosen. Extensive biographical research was conducted on the writers’ mating successes. The first hypothesis was confirmed; the second one, controlling for life age, only for number of mates but not entirely regarding number of children. The latter finding was discussed with respect to, among others, the availability of effective contraception especially in the 20th century. The third hypothesis was not satisfactorily supported. The fourth hypothesis was partially supported. For the 20th century part of the German list, the secondary sex ratio differed with high statistical significance from the ratio assumed to be valid for a general population.

Do individuals in better condition survive for longer? Field survival estimates according to male alternative reproductive tactics and sex

There is a gap in terms of the supposed survival differences recorded in the field according to individual condition. This is partly due to our inability to assess survival in the wild. Here we applied modern statistical techniques to field-gathered data in two damselfly species whose males practice alternative reproductive tactics (ARTs) and whose indicators of condition in both sexes are known. In Paraphlebia zoe, there are two ART: a larger black-winged (BW) male which defends mating territories and a smaller hyaline-winged (HW) male that usually acts as a satellite. In this species, condition in both morphs is correlated with body size. In Calopteryx haemorrhoidalis, males follow tactics according to their condition with males in better condition practicing a territorial ART. In addition, in this species, condition correlates positively with wing pigmentation in both sexes. Our prediction for both species was that males practicing the territorial tactic will survive less longer than males using a nonterritorial tactic, and larger or more pigmented animals will survive for longer. In P. zoe, BW males survived less than females but did not differ from HW males, and not necessarily larger individuals survived for longer. In fact, size affected survival but only when group identity was analysed, showing a positive relationship in females and a slightly negative relationship in both male morphs. For C. haemorrhoidalis, survival was larger for more pigmented males and females, but size was not a good survival predictor. Our results partially confirm assumptions based on the maintenance of ARTs. Our results also indicate that female pigmentation, correlates with a fitness component - survival - as proposed by recent sexual selection ideas applied to females.

Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata)

In a wide range of bird species, females have been shown to express active preferences for males that sing more complex songs. Current sexual selection theory predicts that for this signal to remain an honest indicator of male quality, it must be associated with an underlying cost of development or maintenance. There has been considerable debate questioning the costs associated with song production and learning. Recently, the nutritional stress hypothesis proposed that song complexity could act as an indicator of early developmental history, since the song control nuclei in the brain are laid down early in life. Here we test the nutritional stress hypothesis, by investigating the effects of dietary stress on the quality of adult song produced. In addition, we tested the effects of elevated corticosterone during development on song production to test its possible involvement in mediating the effects of developmental stress. The results demonstrate that both dietary restriction and elevated corticosterone levels significantly reduced nestling growth rates. In addition, we found that experimentally stressed birds developed songs with significantly shorter song motif duration and reduced complexity. These results provide novel experimental evidence that complex song repertoires may have evolved as honest signals of male quality, by indicating early developmental rearing conditions.

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.

Preferences for ultraviolet partners in the blue tit

The preference of female blue tits, Parus caeruleus, is correlated with the brightness of the ultraviolet (UV) crest; there is also assortative mating with respect to the crest's UV/violet chroma. However, manipulation of plumage reflectance is necessary to infer a direct causal link between UV plumage and mate choice. We gave both male and female blue tits a choice between a W-reflecting ('UV+') partner and a partner whose UV plumage reflectance had been removed ('UV-'). Male blue tits significantly preferred UV+ females. Similarly, female blue tits tended to prefer UV-reflecting males, but their UV+ preferences were nonsignificant. Neither sex showed a preference when conspecifics were replaced by a heterospecific. This study suggests mutual mate choice but male choice may be more strongly influenced by the visual appearance of potential mates. This is one of a few studies to show male mate preferences and the first demonstration of a direct relationship between UV reflectance and;male mate choice. (C) 1999 The Association for the Study of Animal Behaviour.

Ultraviolet vision and band-colour preferences in female zebra finches, Taeniopygia guttata

Zebra finches have previously been found to have preferences for particular colours of both natural and artificial traits among opposite sex conspecifics. For example, in some studies female zebra finches preferred males wearing red leg bands to orange-banded and unbanded birds and rejected light green-banded males. In other studies, females also preferred males with red beaks to orange-beaked males. However, several authors have failed to replicate these results. We show that females may fail to show a colour preference because of the absence or removal of ultraviolet light under experimental conditions. In mate-choice trials, females observing males through filters that transmitted ultraviolet preferred red-banded males but where females viewed males through ultraviolet-blocking filters, no such preference was observed. Further investigation revealed that the lack of a colour preference when ultraviolet was absent was probably due to the change in overall appearance of the bird, rather than the change in appearance of the rings themselves. This work highlights the importance of proper consideration of the sensory capabilities of animals in experimental design, particularly with regard to the role of ultraviolet light in avian colour perception. (C) 1997 The Association for the Study of Animal Behaviour.

Iridescent structurally based coloration of eyespots correlates with mating success in the peacock

Gaudy plumage coloration is a widespread ornamental trait in birds and thought to be sexually selected. Although much attention has been devoted to structural coloration reflecting in UV, the signaling function of structural colors lacking UV reflectance and those that exhibit iridescence coloration are poorly documented. The train of the peacock (Pavo cristatus), a classical example of a sexually selected trait, is composed of iridescent structurally colored eyespots not reflecting in UV. Until today, the role played by the structural color of the eyespots in female mate choice has never been investigated using spectrometry. We measured eyespot coloration from a stationary angle (static coloration) and the change in coloration resulting from different angles (iridescent coloration). We assessed coloration with reflectance spectrometry, and we analyzed reflectance spectra using 2 methods. First, we extracted the reflectance spectra shape descriptors hue, brightness, and chroma. Second, we computed color and brightness contrasts signaled by eyespot feathers, taking peafowl color visual sensitivity into account. Iridescence was estimated by the maximal change for all parameters. Brightness was correlated with male mating success. The maximal change in color contrast was correlated with both the frequency of male visitation by females and male mating success. These results suggest that peahens can use both static and dynamic (i.e., iridescent) aspects of plumage structural coloration as signals to detect and choose their mates.

Rapid behavioural adjustments to unfavourable light conditions in European starlings (Sturnus vulgaris)

Although it is known that many birds possess ultraviolet (UV)-sensitive vision, most commercially housed poultry species, as well as species held in zoos, laboratories, or bred for show, are maintained under lighting that is deficient in UV wavelengths compared with normal daylight. UV-sensitive vision has been shown to be important in both foraging and mate-choice decisions. UV-poor conditions, in which information in this waveband is eliminated, could, therefore, present an important welfare issue. Eight European starlings were given a series of preference tests (eight hours per trial, for six days), in which they could choose to feed in one of four channels. Four experimental trials were carried out, during which the channels were covered in either UV-transmitting (UV+) or UV-blocking (UV-) filters, to determine whether birds had an initial preference for feeding in UV-rich environments and whether there was any change in their preference over time. There was an initial preference for the UV+ environment, but this preference declined very rapidly with familiarity, and was absent by the final trial. These results imply that starlings can rapidly adjust their feeding behaviour if faced with unfamiliar light environments and that any initial behavioural changes attributable to UV-deficient environments may be short-lived. However, further work is necessary to establish whether these adjustments occur across a range of species and contexts before any welfare concerns can be ruled out.

The spatial pattern of natural selection when selection depends upon experience

Apostatic (frequency‐ or density‐dependent) selection, aposematic signals, and mate choice behavior generally require that the mean prey or potential mate density m value be high enough (above a threshold T) to result in sufficient encounter rates for the searcher to learn or retain the association between conspicuous signals and prey unprofitability, to forage apostatically, or to choose among mates. This assumes that all searchers experience , which implicitly assumes an even dispersion of targets among searcher territories. Uneven dispersion generates new phenomena. If , then only territories with local density x values that are greater than T favor experience‐based behavior, leading to spatially variable frequency‐ or density‐dependent selection intensity. As aggregation increases, the increase in percentage of targets in favorable territories ( ) is greater than the increase in the percentage of territories that are favorable. The relationship is reversed when . In both cases, because as few as 10% of the territories can contain 80% of the targets, only a few territory holders may account for most of the selection on most of the target population; accidents of experience in only a few searchers can have unexpectedly large effects on the target population. This also provides an explanation for high searcher behavior variation (personalities) : individuals from favorable territories will behave differently in behavioral experiments than those from unfavorable territories, at least with respect to similar kinds of targets. These effects will generate spatial heterogeneity in natural and sexual selection in what are otherwise uniform environments.

Environmental variation and the maintenance of polymorphism : the effect of ambient light spectrum on mating behaviour and sexual selection in guppies

The intensity of sexual selection is influenced by environmental conditions because these conditions influence signal propagation and the risks of the signal being exploited by predators and parasites. We explore the possibility that spatial or temporal heterogeneity in environmental signalling conditions (in this case light spectrum) may induce fluctuating sexual selection on male behaviour and ornamentation in guppies. We used shade cloth and filters to experimentally manipulate light spectrum, mimicking conditions found naturally: early morning/late afternoon light (SC treatment), midday forest shade (F89 filter treatment) and midday woodland shade (F55 filter treatment). Females were more responsive to male courtship and males were less likely to attempt sneak copulations under F55 light than the other two treatments. By contrast, male display rate was not influenced by treatment. Females tended to prefer the same males under SC and F55 light, but attractiveness in these treatments was unrelated to attractiveness under F89 light. There were similarities among treatments in the traits that females preferred: females preferred males with larger areas of orange in all three treatments. There were, however, also some differences, including preference for larger males under F89 light and for smaller males under the other treatments. Overall, the influence of ambient light spectrum on the relative importance of mate choice and male sneak copulation may have important implications for the mode and strength of sexual selection in different environments. The findings on attractiveness and preference functions, however, suggest that light spectrum only weakly affects the direction of sexual selection by female choice.

Sperm competition and offspring viability at hybridization in Australian tree frogs, Litoria peronii and L. tyleri

Hybridization between closely related species often leads to reduced viability or fertility of offspring. Complete failure of hybrid offspring (post-zygotic hybrid incompatibilities) may have an important role in maintaining the integrity of reproductive barriers between closely related species. We show elsewhere that in Peron's tree frog, Litoria peronii, males more closely related to a female sire more offspring in sperm competition with a less related rival male. Observations of rare 'phenotypic intermediate' males between L. peronii and the closely related L. tyleri made us suggest that these relatedness effects on siring success may be because of selection arising from risks of costly hybridization between the two species. Here, we test this hypothesis in an extensive sperm competition experiment, which shows that there is no effect of species identity on probability of fertilization in sperm competition trials controlling for sperm concentration and sperm viability. Instead, there was a close agreement between a male's siring success in isolation with a female and his siring success with the same female in competition with a rival male regardless of species identity. Offspring viability and survival, however, were strongly influenced by species identity. Over a 14-day period, hybrid offspring suffered increasing mortality and developed more malformations and an obvious inability to swim and right themselves, leading to compromised probability of survival. Thus, hybridization in these sympatric tree frogs does not compromise fertilization but has a strong impact on offspring viability and opportunity for reinforcement selection on mate choice for conspecific partners.

The functional significance of multiple nest-building in the Australian Reed Warbler Acrocephalus australis

The vast majority of bird species build a nest in which to breed. Some species build more than one nest, but the function of most multiple nest-building remains unclear. Here we describe the unusual nest-building behaviour of the Australian Reed Warbler Acrocephalus australis, and test experimentally the hypotheses that multiple nest-building is related to individual condition or territory quality, and plays a role in mate assessment. Australian Reed Warblers built two types of nest structures: 'type I' nests, which were used for eggs and nestlings, and 'type II' nests, which were structurally distinct from type I nests, did not support eggs, nestlings or adults and were not essential for successful breeding. The number of type II nests built in each territory varied. Type II nests were only built before breeding had commenced in a territory and females were not observed participating in their construction, supporting a role in female mate choice. Birds provided with supplementary food built significantly more type II nests than control birds. However, supplementary-fed birds did not have greater pairing success, and the addition of further type II nests to territories did not increase the pairing rate or type II nest construction in those territories. There was no relationship between the presence of type II nests and either reproductive success or likelihood of nest predation. We discuss the implications of these results in light of previous suggestions regarding the function of multiple nest-building in birds.

Is extrapair mating random? On the probability distribution of extrapair young in avian broods

A dichotomy in female extrapair copulation (EPC) behavior, with some females seeking EPC and others not, is inferred if the observed distribution of extrapair young (EPY) over broods differs from a random process on the level of individual offspring (binomial, hypergeometrical, or Poisson). A review of the literature shows such null models are virtually always rejected, with often large effect sizes. We formulate an alternative null model, which assumes that 1) the number of EPC has a random (Poisson) distribution across females (broods) and that 2) the probability for an offspring to be of extrapair origin is zero without any EPC and increases with the number of EPC. Our brood-level model can accommodate the bimodality of both zero and medium rates of EPY typically found in empirical data, and fitting our model to EPY production of 7 passerine bird species shows evidence of a nonrandom distribution of EPY in only 2 species. We therefore argue that 1) dichotomy in extrapair mate choice cannot be inferred only from a significant deviation in the observed distribution of EPY from a random process on the level of offspring and that 2) additional empirical work on testing the contrasting critical predictions from the classic and our alternative null models is required.

The evolution of plumage colouration in parrots : a review

The plumages of parrots provide some of the most striking colouration in nature.We summarise the diversity of mechanisms producing colour in parrots and the current evidence for the adaptive significance of variation in the colour of parrot plumages. Only recently have detailed studies begun to unravel the mechanisms of their colour-production and colour vision systems. Parrots produce much of their plumage colouration through a unique suite of pigments (psittacofulvins), or through a feather tissue nanostructure that results in coherent scattering of light, or a combination of the two (producing green). Psittacofulvins are found nowhere else in nature, and may even generate fluorescence in many parrot species.Compared with other avian taxa, the adaptive significance of parrot plumage colouration remains poorly understood, although some studies suggest that plumage colouration may form important sexual signals and may be used in mate-choice by several species. There is evidence to suggest that parrot colouration can be subject to both environmental and genetic control. We emphasise that parrots offer a distinctive and useful colouration system for further study. Further research is required to unravel how the dramatic colour patterns of parrots evolved, and what roles colour signals may play in the life histories of parrots.

Great bowerbirds create theaters with forced perspective when seen by their audience

Birds in the infraorder Corvida [1] (ravens, jays, bowerbirds) are renowned for their cognitive abilities [2–4], which include advanced problem solving with spatial inference [4–8], tool use and complex constructions [7–10], and bowerbird cognitive ability is associated with mating success [11]. Great bowerbird males construct bowers with a long avenue from within which females view the male displaying over his bower court [10]. This predictable audience viewpoint is a prerequisite for forced (altered) visual perspective [12–14]. Males make courts with gray and white objects that increase in size with distance from the avenue entrance. This gradient creates forced visual perspective for the audience; court object visual angles subtended on the female viewer’s eye are more uniform than if the objects were placed at random. Forced perspective can yield false perception of size and distance [12, 15]. After experimental reversal of their size-distance gradient, males recovered their gradients within 3 days, and there was little difference from the original after 2 wks. Variation among males in their forced-perspective quality as seen by their female audience indicates that visual perspective is available for use in mate choice, perhaps as an indicator of cognitive ability. Regardless of function, the creation and maintenance of forced visual perspective is clearly important to great bowerbirds and suggests the possibility of a previously unknown dimension of bird cognition.