Rapid evolution by sexual selection in a wild, invasive mammal.

Sexual selection theory provides a framework for investigating the evolution of traits involved in attracting and competing for mates. Given the sexual function of such traits, studies generally focus on individual interactions (i.e., displays and contests) in explaining trait origin and persistence. We show that ecological factors can strongly influence the adaptive value of these traits, and changes to these factors can lead to rapid evolutionary change. We compared sexually selected traits in the small Indian mongoose (Urva auropunctata) between their sparsely populated native range and four tropical islands to which they were introduced within the last 150 years and where, due to a lack of interspecific competition and predation, they have become invasive and densely populated. Because of a likely increase in encounter rate, we predicted that selection on long-distance chemical advertisement by males would relax in the introduced range. Accordingly, male, but not female, anal pads (used in scent marking) decreased in size in relation to both time since introduction and population density, and their relationship to body size and condition weakened. Concurrently, as predicted by intensified sperm competition, testis size increased following introduction. The small Indian mongoose thus experienced an inversion in the relative contributions to fitness of two sexual traits, followed by their rapid evolution in line with ecological changes.

Shedding Light on Bird Egg Color: Pigment as Parasol and the Dark Car Effect.

The vibrant colors of many birds' eggs, particularly those that are blue to blue-green, are extraordinary in that they are striking traits present in hundreds of species that have nevertheless eluded evolutionary functional explanation. We propose that egg pigmentation mediates a trade-off between two routes by which solar radiation can harm bird embryos: transmittance through the eggshell and overheating through absorbance. We quantitatively test four components of this hypothesis on variably colored eggs of the village weaverbird (Ploceus cucullatus) in a controlled light environment: (1) damaging ultraviolet radiation can transmit through bird eggshells, (2) infrared radiation at natural intensities can heat the interior of eggs, (3) more intense egg coloration decreases light transmittance ("pigment as parasol"), and (4) more intense egg coloration increases absorbance of light by the eggshell and heats the egg interior ("dark car effect"). Results support all of these predictions. Thus, in sunlit nesting environments, less pigmentation will increase the detrimental effect of transmittance, but more pigmentation will increase the detrimental effect of absorbance. The optimal pigmentation level for a bird egg in a given light environment, all other things being equal, will depend on the balance between light transmittance and absorbance in relation to embryo fitness.

Light dulls and darkens bird eggs.

Although egg color is generally consistent within individual birds and robust to environmental variation, recent evidence suggests a degree of susceptibility to environmental perturbation or modulation of egg color. Most of this variation manifests via the physiology of the laying female, but some direct impacts of the environment on laid eggs have also been discovered. Here we test whether light changes bird egg color and we quantify its effect, by subjecting variable blue-green eggs of Rüppell's weaver (Ploceus galbula) to a broad-spectrum light source under laboratory conditions, and measuring egg reflectance every few hours. Eggshells gradually decreased in reflectance across the entire measured wavelength spectrum of 250-800 nm. Reflectance peaks were disproportionately affected, such that the height decreased of both the blue-green peak and the smaller UV peak typical of blue-green eggs. The reflectance of lighter eggs was affected slightly more than that of darker eggs. These changes are similar to previous results for changes over long periods of time in darkness, suggesting that light might hasten the same process of pigment degradation that proceeds even without light. Comparison between the experimental light source and both sunlight and typical artificial lighting situations raises the possibility that significant color change might occur during incubation in some birds, but indicates that eggshell illumination in museums for short periods of study is unlikely to affect their color to a detectable extent. Additional research should be performed on eggs of other species and in other light environments, with an eye to an eventual generalized model of the effect of light on eggshell color.

Quantitative integration of genetic factors in the learning and production of canary song.

Learned bird song is influenced by inherited predispositions. The canary is a model system for the interaction of genes and learning on behaviour, especially because some strains have undergone artificial selection for song. In this study, roller canaries (bred for low-pitched songs) and border canaries (whose song is higher pitched, similar to the wild-type) were interbred and backcrossed to produce 58 males that sorted into seven genetically distinct groups. All males were tutored with the same set of songs, which included both low- and high-pitched syllables. Individuals were consistent within genetic groups but differed between groups in the proportion of low- versus high-pitched syllables they learned and sang. Both sex-linked and autosomal factors affected song learning and song production, in an additive manner. Dominant Z-chromosome factors facilitated high-pitched syllable learning and production, whereas the sex-linked alleles associated with the switch to low-pitched syllables under artificial selection were largely recessive. With respect to autosomal effects, the most surprising result is that males in the same genetic group had almost identical repertoires. This result challenges two common preconceptions: that genetic changes at different loci lead to distinct phenotypic changes, and that genetic predispositions affect learning in simple and general ways. Rather, different combinations of genetic changes can be associated with the same phenotypic effect; and predispositions can be remarkably specific, such as a tendency to learn and sing one song element rather than another.

Responses to song playback vary with the vocal performance of both signal senders and receivers.

Mating signals of many animal species are difficult to produce and thus should indicate signaler quality. Growing evidence suggests that receivers modulate their behaviour in response to signals with varying performance levels, although little is known about if and how responses are affected by receiver attributes. To explore this topic we conducted two experiments with swamp sparrows, Melospiza georgiana, in which we challenged territorial males with playback of songs with trill rates that were natural, digitally reduced, or digitally elevated (control-, low- and high-performance stimuli, respectively). In our first experiment, we found that males responded more aggressively to control songs than to low-performance stimuli, that low-performance stimuli with the most severe trill-rate reductions elicited the weakest aggressive responses, and that the subjects' own trill rates predicted aggressive responses. In our second experiment, we found that male responses to high-performance stimuli varied significantly, in ways predicted by two factors: the degree to which we had elevated stimulus performance levels of high-performance stimuli, and subjects' own vocal performance levels. Specifically, males were less aggressive towards stimuli for which we had elevated performance levels to higher degrees, and subject males with higher vocal performances themselves responded more aggressively. These findings together offer a novel illustration of how responses to aggressive signals may rely not just on signal attributes, but also on attributes of responding animals themselves.

Relaxed selection in the wild.

Natural populations often experience the weakening or removal of a source of selection that had been important in the maintenance of one or more traits. Here we refer to these situations as 'relaxed selection,' and review recent studies that explore the effects of such changes on traits in their ecological contexts. In a few systems, such as the loss of armor in stickleback, the genetic, developmental and ecological bases of trait evolution are being discovered. These results yield insights into whether and how fast a trait is reduced or lost under relaxed selection. We provide a prospectus and a framework for understanding relaxed selection and trait loss in natural populations. We also examine its implications for applied issues, such as antibiotic resistance and the success of invasive species.

Persistence of egg recognition in the absence of cuckoo brood parasitism: pattern and mechanism.

Broad ecological shifts can render previously adaptive traits nonfunctional. It is an open question as to how and how quickly nonfunctional traits decay once the selective pressures that favored them are removed. The village weaverbird (Ploceus cucullatus) avoids brood parasitism by rejecting foreign eggs. African populations have evolved high levels of within-clutch uniformity as well as individual distinctiveness in egg color and spotting, a combination that facilitates identification of foreign eggs. In a companion study, I showed that these adaptations in egg appearance declined following introductions of weavers into habitats devoid of egg-mimicking brood parasites. Here, I use experimental parasitism in two ancestral and two introduced populations to test for changes in egg rejection behavior while controlling for changes in egg appearance. Introduced populations reject foreign eggs less frequently, but the ability of source and introduced populations to reject foreign eggs does not differ after controlling for the evolution of egg color and spotting. Therefore, egg rejection behavior in introduced populations of the village weaver has been compromised by changes in egg appearance, but there has been no significant decline in the birds' ability to recognize foreign eggs. This result reconciles earlier studies on this system and provides insights into the ways behavior can change over generations, especially in the context of recognition systems and the avoidance of brood parasitism.

Evolution of bird eggs in the absence of cuckoo parasitism.

Historical introductions of species into new habitats can create rare opportunities to test evolutionary hypotheses, such as the role of natural selection in maintaining traits. This study examines two independent introductions of the African village weaverbird (Ploceus cucullatus) to islands where selection on egg appearance traits is expected to differ markedly from that of the source populations. The color and spotting of village weaver eggs in Africa are highly consistent within clutches, but highly variable between individuals. These two features may be an evolutionary response to brood parasitism. In Africa, weavers are parasitized by each other and by the diederik cuckoo (Chrysococcyx caprius), an egg mimic. African village weavers were introduced one century ago to Mauritius, and over two centuries ago to Hispaniola. Both islands are devoid of egg-mimicking brood parasites. In these two populations, between-individual variation and within-clutch consistency in egg appearance have both decreased, as has the incidence of spotting, relative to the source populations in Africa. These reductions are more pronounced on Hispaniola, the earlier introduction. Such changes support the hypothesis that egg appearance in the African village weaver has been maintained by natural selection as a counteradaptation to cuckoo brood parasitism. These results illustrate that the removal of an agent of selection can sometimes bring about rapid evolutionary consequences.