Variation in the Non-mimetic Vocalizations of Brood-Parasitic Indigobirds and Their Potential Role in Speciation

Indigobirds (Vidua spp.) are obligate brood parasites in which imprinting on heterospecific hosts shapes adult vocal behavior and mating preferences. Adult male indigobirds mimic the songs and other vocalizations of their respective hosts, which signals their own host environment to prospective mates and has important implications for speciation. In this study, we examined variation within and among indigobird species in the non-mimetic components of their vocal behavior, including both chatter calls and their impressive repertoires of intricate non-mimicry songs. We test whether indigobird species in Tanzania (V. chalybeata, V. codringtoni, V. funerea, and V. purpurascens) differ consistently in general features of their non-mimetic vocalizations, and we test whether local ecological conditions influence vocal behavior. Indigobird non-mimetic song repertories are learned from and shared with other males of the same species. We find that local dialect “neighborhoods” are variable in size among species and regions, depending on habitat continuity and the distribution of male territories. Despite the complete turnover of the specific songs comprising non-mimicry song repertoires from one local dialect to the next, we find significant species effects for more general measures of non-mimicry songs such as repertoire size and diversity, frequency, song length, and pace. For some traits, we also found significant regional differences, which may be mediated by significant relationships between elevation and morphometrics. Chatter calls were broadly similar across both species and localities, but we found significant species and region effects for frequency and to a lesser extent pace. We discuss the possibility that learning and mimicking the vocalizations of different hosts might influence the production of non-mimetic vocalizations and explain many of the species differences we detected. Whether these species differences are purely due to phenotypic plasticity or also reflect genetic divergence in traits influencing sound production and/or female preferences, they may contribute to reproductive isolation among nascent and recently evolved indigobird species.

Female preferences for male golden snub-nosed monkeys vary with male age and social context

Age is a key factor affecting sexual selection, as many physical and social traits are age-related. Although studies of primate mate choice often consider particular age-related traits, few consider the collective effects of male age. We tested the hypothesis that female golden snub-nosed monkeys Rhinopithecus roxellana prefer prime aged males (10–15 years) over younger and older males. We examined a habituated, provisioned troop during a 3-year study in the Qinling Mountains, China. Prime age males were more likely to be resident males of one-male units (OMUs) than males of other ages. Since females are free to transfer between OMUs, the number of females per OMU can be indicative of female preferences. We examined the number of females per OMU, and found that it increased with resident male age up to 7–8 years, and declined after 12 years, such that prime age resident males had more females than other resident males. Females also initiated extra-unit copulations with high-ranking prime age males at significantly higher rates than with other males. Nevertheless, females tended to transfer from OMUs with high-ranking, older resident males to those with lower-ranking, younger resident males. Thus, females appear to use different strategies when choosing social mates and extra-unit mates (i.e., different social contexts). We speculate that females may perceive early signs of aging in males and trade off the benefits and costs of high rank vs. male senescence. This study lays the groundwork for future studies that examine possible direct and indirect benefits of such strategies.

Darwin, sexual selection, and the brain

One hundred fifty years ago Darwin published The Descent of Man, and Selection in Relation to Sex, in which he presented his theory of sexual selection with its emphasis on sexual beauty. However, it was not until 50 y ago that there was a renewed interest in Darwin’s theory in general, and specifically the potency of mate choice. Darwin suggested that in many cases female preferences for elaborately ornamented males derived from a female’s taste for the beautiful, the notion that females were attracted to sexual beauty for its own sake. Initially, female mate choice attracted the interest of behavioral ecologists focusing on the fitness advantages accrued through mate choice. Subsequent studies focused on sensory ecology and signal design, often showing how sensory end organs influenced the types of traits females found attractive. Eventually, investigations of neural circuits, neurogenetics, and neurochemistry uncovered a more complete scaffolding underlying sexual attraction. More recently, research inspired by human studies in psychophysics, behavioral economics, and neuroaesthetics have provided some notion of its higher-order mechanisms. In this paper, I review progress in our understanding of Darwin’s conjecture of “a taste for the beautiful” by considering research from these diverse fields that have conspired to provide unparalleled insight into the chooser’s mate choices.

Female preferences for discrete and continuous male colour expression may help reinforce colour polymorphism in a desert lizard

Despite recognition that colour can vary continuously, colour expression in colour polymorphic species is usually treated as discrete. We conducted three experiments to evaluate the extent that discrete and continuous male coloration influenced female mating preferences in long-tailed brush lizards (Urosaurus graciosus). Each experiment provided females with a different social context: a dimorphic choice between a yellow and an orange male (coloration treated as discrete), and a choice between either two orange males or two yellow males (coloration treated as continuous variation). Females preferred orange males over yellow males in the first experiment, and the findings of our second experiment suggested that males with moderate orange coloration were most preferred. In contrast, females behaved randomly with respect to two yellow males. Our findings show that females in colour polymorphic species can evaluate both discrete and continuous aspects of morph coloration during mate assessment, which may help maintain their polymorphism.

Olfactory Choice for Decomposition Stage in the Burying Beetle Nicrophorus vespilloides: Preference or Aversion?

Sensory cues predicting resource quality are drivers of key animal behaviors such as preference or aversion. Despite the abundance of behavioral choice studies across the animal kingdom, relatively few studies have tested whether these decisions are driven by preference for one choice or aversion to another. In the burying beetle Nicrophorus vespilloides, adult pairs exhibit parental care to raise their offspring on a small carrion resource. We tested whether carrion decomposition stage affected brood quantity and quality and found that mating pairs had significantly more offspring on fresher carcasses. To determine whether this observed reproductive benefit correlates with maternal preference behavior, we conducted a series of olfactory trials testing mated female preferences for mouse carcasses of differing decomposition stages. When given the option between fresh and older carcasses, females associated significantly more with fresher, 1-day old carcasses. However, this behavior may be driven by aversion, as females that were given a choice between the 7-day old carcass and a blank control spent significantly more time in the control chamber. We characterized volatile organic compound profiles of both carcass types, highlighting unique compounds that may serve as public information (sensu lato) conveying resource quality information to gravid beetles.

The role of boundary length and adjacent patch contrast in guppy mate choice

The presence of various combinations of adjacent colors within polymorphic species’ color pattern could have a major impact on mate choice. We studied the role of pattern geometry in predicting mate choice in guppies using boundary strength analysis (BSA). BSA estimates the visual contrast intensity between two adjacent color patches (ΔS) weighted by the lengths of the boundaries between these adjacent color patches. We measured both the chromatic (hue and saturation) and achromatic (luminance) ΔS for each pair of adjacent patches. For each male’s color pattern, we measured BSA as both mean (mΔS) and coefficient of variation (cvΔS) of all ΔS weighted by their corresponding boundary lengths. We also determined if specific color patch boundaries had an impact on female preferences and whether these predicted overall male contrast (mΔS). We found that males with a higher mΔS were more attractive to females and that six boundaries containing either fuzzy black or black as one of the pair colors significantly affected female preferences, indicating that 1) females favored highly conspicuous males and 2) melanin-based patches could be used as a signal amplifier, not only for orange but for other colors.

Male–male contest limits the expression of assortative mate preferences in a polymorphic poison frog

Codivergence of sexual traits and mate preferences can lead to assortative mating and subsequently reproductive isolation. However, mate choice rarely operates without intrasexual competition, and the effects of the latter on speciation are often overlooked. Maintaining trait polymorphisms despite gene flow and limiting assortative female preferences for less-competitive male phenotypes are two important roles that male–male competition may play in the speciation process. Both roles rely on the assumption that male–male competition limits the expression of divergent female preferences. We tested this assumption in the highly color-polymorphic strawberry poison frog (Oophaga pumilio). Females prefer males of the local color, suggesting that reproductive isolation may be evolving among color morphs. However, this inference does not account for male–male competition, which is also color-mediated. We housed females with two differently colored males, and compared reproductive patterns when the more attractive male was the territory holder versus when he was the nonterritorial male. Females mated primarily with the territory winner, regardless of coloration, suggesting that when a choice must be made between the two, male territoriality overrides female preferences for male coloration. Our results highlight the importance of considering the combined effects of mate choice and intrasexual competition in shaping phenotypic divergence and speciation.

The ecological stage changes benefits of mate choice and drives preference divergence

Preference divergence is thought to contribute to reproductive isolation. Ecology can alter the way selection acts on female preferences, making them most likely to diverge when ecological conditions vary among populations. We present a novel mechanism for ecologically dependent sexual selection, termed ‘the ecological stage’ to highlight its ecological dependence. Our hypothesized mechanism emphasizes that males and females interact over mating in a specific ecological context, and different ecological conditions change the costs and benefits of mating interactions, selecting for different preferences in distinct environments and different male traits, especially when traits are condition dependent. We test key predictions of this mechanism in a sympatric three-spine stickleback species pair. We used a maternal half-sib split-clutch design for both species, mating females to attractive and unattractive males and raising progeny on alternate diets that mimic the specialized diets of the species in nature. We estimated the benefits of mate choice for an indicator trait (male nuptial colour) by measuring many fitness components across the lifetimes of both sons and daughters from these crosses. We analysed fitness data using a combination of aster and mixed models. We found that many benefits of mating with high-colour males depended on both species and diet. These results support the ecological stage hypothesis for sticklebacks. Finally, we discuss the potential role of this mechanism for other taxa and highlight its ability to enhance reproductive isolation as speciation proceeds, thus facilitating the evolution of strong reproductive isolation. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.

Strong sexual selection despite spatial constraints on extrapair paternity

Extrapair paternity should contribute to sexual selection by increasing the number of potential mates available to each individual. Potential copulation partners are, however, limited by their proximity. Spatial constraints may therefore reduce the impact of extrapair paternity on sexual selection. We tested the effect of spatial constraints on sexual selection by simulating extrapair copulations for 15 species of socially monogamous songbirds with varying rates of extrapair paternity. We compared four metrics of sexual selection between simulated populations without spatial constraints and populations where extrapair copulations were restricted to first- and second-order neighbors. Counter to predictions, sexual selection as measured by the Bateman gradient (the association between the number of copulation partners and offspring produced) increased under spatial constraints. In these conditions, repeated extrapair copulations between the same individuals led to more offspring per copulation partner. In contrast, spatial constraints did somewhat reduce sexual selection—as measured by the opportunity for selection, s’max, and the selection gradient on male quality—when the association between simulated male quality scores and copulation success (e.g., female preferences or male–male competition) was strong. Sexual selection remained strong overall in those populations even under spatial constraints. Spatial constraints did not substantially reduce sexual selection when the association between male quality and copulation success was moderate or weak. Thus, spatial constraints on extrapair copulations are insufficient to explain the absence of strong selection on male traits in many species.