Low frequency groans indicate larger and more dominant fallow deer (Dama dama) males

Background

Models of honest advertisement predict that sexually selected calls should signal male quality. In most vertebrates, high quality males have larger body sizes that determine higher social status and in turn higher reproductive success. Previous research has emphasised the importance of vocal tract resonances or formant frequencies of calls as cues to body size in mammals. However, the role of the acoustic features of vocalisations as cues to other quality-related phenotypic characteristics of callers has rarely been investigated.

Methodology/Principal Findings

We examined whether the acoustic structure of fallow deer groans provides reliable information on the quality of the caller, by exploring the relationships between male quality (body size, dominance rank, and mating success) and the frequency components of calls (fundamental frequency, formant frequencies, and formant dispersion). We found that body size was not related to the fundamental frequency of groans, whereas larger males produced groans with lower formant frequencies and lower formant dispersion. Groans of high-ranking males were characterised by lower minimum fundamental frequencies and to a lesser extent, by lower formant dispersions. Dominance rank was the factor most strongly related to mating success, with higher-ranking males having higher mating success. The minimum fundamental frequency and the minimum formant dispersion were indirectly related to male mating success (through dominance rank).

Conclusion/Significance

Our study is the first to show that sexually selected vocalisations can signal social dominance in mammals other than primates, and reveals that independent acoustic components encode accurate information on different phenotypic aspects of male quality.     

Calling,Courtship, and Condition in the Fall Field Cricket,Gryllus pennsylvanicus

Theoretically, sexual signals should provide honest information about mating benefits and many sexually reproducing species use honest signals when signalling to potential mates. Male crickets produce two types of acoustic mating signals: a long-distance mate attraction call and a short-range courtship call. We tested whether wild-caught fall field cricket (Gryllus pennsylvanicus) males in high condition (high residual mass or large body size) produce higher effort calls (in support of the honest signalling hypothesis). We also tested an alternative hypothesis, whether low condition males produce higher effort calls (in support of the terminal investment hypothesis). Several components of long-distance mate attraction calls honestly reflected male body size, with larger males producing louder mate attraction calls at lower carrier frequencies. Long-distance mate attraction chirp rate dishonestly signalled body size, with small males producing faster chirp rates. Short-range courtship calls dishonestly reflected male residual mass, as chirp rate and pulse rate were best explained by a curvilinear function of residual mass. By producing long-distance mate attraction calls and courtship calls with similar or higher effort compared to high condition males, low condition males (low residual mass or small body size) may increase their effort in current reproductive success at the expense of their future reproductive success, suggesting that not all sexual signals are honest.     

Free‐Ranging Red Deer Hinds Show Greater Attentiveness to Roars with Formant Frequencies Typical of Young Males

Acoustic cues present in the reproductive calls of many animal species potentially encode important information about the caller. Here, we test the response of a free‐ranging population of peri‐oestrus red deer hinds to variation in a specific acoustic cue to body size in the male roar, the formant frequencies. Our results revealed: (1) that hinds showed greater overall attention (judged by longer looking responses and lower response latencies) to roars simulating males of sub‐adult body size than to those simulating a large adult male and (2) that hinds without dependent offspring had greater looking responses to male roars and lower response latencies than hinds with dependent offspring to roars simulating sub‐adult males. These findings indicate that free‐ranging red deer hinds may use formants as acoustic cues to gauge the body size and maturity of males in their natural environment, possibly to facilitate earlier detection and avoidance of young stags that are known to harass them.     

Great expectations: dominance,breeding success and offspring sex ratios in red deer

Differences in dominance rank among red deer (Cervus elaphus) females (hinds) on Rhum were related to their breeding success as well as to the comparative success of male and female offspring. Males (stags) born to mothers above median rank were more successful than hinds, while hinds born to subordinate mothers were more successful than stags. The ratio of male to female calves produced by dominant mothers was significantly higher than that produced by subordinates. Since dominance rank among hinds is related to their body weight as adults and to their birth weight, these results suggest that the birth sex ratio may be affected by environmental factors operating during a female's early development.     

Estrous female goats use testosterone-dependent cues to assess mates

In a promiscuous species like the domestic goat (Capra hircus), in which maternal investment is greater than paternal investment, a female may mate selectively with a more-fit male to improve her reproductive fitness. Testosterone (T) controls a large suite of male-typical behaviors and morphological characteristics. High T concentrations may be energetically costly or even detrimental to survival; thus, preventing lower quality males from falsely advertising their fitness. Three preference studies were conducted to examine if females use T-dependent cues to assess potential mates. For Experiment 1, females were given a choice between a pair of morphologically similar males, bucks (intact males) and stags (post-pubertally castrated males), during the breeding and non-breeding seasons. In both seasons, females preferred the bucks compared to stags. In Experiment 2, females were given a choice between bucks, stags and wethers (pre-pubertally castrated males) during the non-breeding season. For some comparisons, castrated males received 25 mg testosterone propionate (TP) or were untreated. Females preferred TP-treated males compared to untreated males and showed no preference when given a choice between either two TP-treated or two untreated males. In Experiment 3, females were given a choice between a pair of bucks and a pair of stags treated with 25 mg TP during monthly tests in the breeding season. At each monthly test, females preferred the males with higher T concentrations near the time of the behavior test. These studies suggest that females use T-dependent cues to assess potential mates, and T concentrations may indicate a male's overall fitness.     

Sexual Selection in the Loud Calls of Male Primates: Signal Content and Function

Researchers have used sexual selection theory and hypotheses based on intersexual mate choice and intrasexual mate competition to explain the role of spontaneous long-distance vocalizations emitted by adult male primates, relying on the tacit assumption that assessment or identity cues are encoded in the vocalizations. I review the published literature and aim to substantiate a relationship between sexual selection and long-distance vocal communication in primates. First, I review findings from nonprimate taxa to determine the relative importance of inter- and intrasexual selection and to provide a background for examining primates. Next, I describe several hypotheses for signal content and function in adult male loud calls. Then, I examine the available data across Primates for evidence to support or to refute these hypotheses and to determine if they meet proposed criteria for demonstrating sexual selection [Snowdon, C. T. (2004). Sexual Selection in Primates: New and Comparative Perspectives]. Signal content refers to patterns of acoustic features within vocalizations from which listeners might extract cues or information about the signaler. I interpret signal function, in turn, from behavioral responses of receivers and assume it has ultimate effects on the evolution and design of acoustic signals if direct fitness consequences exist. After the general review across primates, I propose orangutans as a candidate species for further evaluation of sexual selection in vocal communication. The available evidence corroborates a demonstrable relationship between sexual selection and adult male loud calls based on individual recognition, but it is necessary to obtain additional data to affirm a direct benefit to reproductive success.     

Formant Frequencies are Acoustic Cues to Caller Discrimination and are a Weak Indicator of the Body Size of Corncrake Males

Source–filter theory assumes that calls are generated by a vocal source and are subsequently filtered by the vocal tract. The air in the vocal tract vibrates preferentially at certain resonant frequencies, called formants. Formant frequencies can be a good indicator of the caller's characteristics, such as sex, age, body size or individual identity. Although source–filter theory was originally proposed for mammals, formants are also observed in birds, and some bird species have been shown to perceive formants. In this study, we evaluated the hypotheses that formant frequencies (1) are an indicator of body size and (2) can be used for individual discrimination by a nocturnal bird species, the corncrake (Crex crex). We analysed calls of 104 males from Poland and the Czech Republic. Linear regression models showed that the males with a longer head (including the bill length) had a significantly lower formant dispersion and lower fourth and fifth formant frequencies. However, we found no significant relationships between body weight and any filter‐related acoustic measurement. The formant frequencies had smaller within‐ than between‐individual coefficients of variation. This characteristic of the formant frequencies implies a high potential for individual coding. A discriminant function analysis correctly assigned 94.8% of the calls to the caller based on formants from second to fifth. Our results indicated that the formant frequencies are a weak indicator of the body size of the sender in the corncrake. However, even weak dependence between body size and acoustic properties of signal may be important in natural selection process. Alternatively, such a weak dependence may be observed, because receivers ignore the acoustical, formant‐based cues of body size. Simultaneously, the formants might potentially provide acoustic cues to individual discrimination and could be used to census and monitoring tasks.     

Vocal Tract Morphology Determines Species-Specific Features in Vocal Signals of Lemurs (Eulemur)

The source-filter theory describes vocal production as a two-stage process involving the generation of a sound source, with its own spectral structure, which is then filtered by the resonant properties of the vocal tract. This theory has been successfully applied to the study of animal vocal signals since the 1990s. As an extension, models reproducing vocal tract resonance can be used to reproduce formant patterns and to understand the role of vocal tract filtering in nonhuman vocalizations. We studied three congeneric lemur species —Eulemur fulvus, E. macaco, E. rubriventer— using morphological measurements to build computational models of the vocal tract to estimate formants, and acoustic analysis to measure formants from natural calls. We focused on call types emitted through the nose, without apparent articulation. On the basis of anatomical measurements, we modeled the vocal tract of each species as a series of concatenated tubes, with a cross-sectional area that changed along the tract to approximate the morphology of the larynx, the nasopharyngeal cavity, the nasal chambers, and the nostrils. For each species, we calculated the resonance frequencies in 2500 randomly generated vocal tracts, in which we simulated intraspecific length and size variation. Formant location and spacing showed significant species-specific differences determined by the length of the vocal tract. We then measured formants of a set of nasal vocalizations (“grunts”) recorded from captive lemurs of the same species. We found species-specific differences in the natural calls. This is the first evidence that morphology of the vocal tract is relevant in generating filter-related acoustic cues that potentially provide receivers with information about the species of the emitter.     

Is the colour dimorphism inDactylorhiza sambucina maintained by differential seed viability instead of frequency-dependent selection?

The European rewardless, bee-pollinated orchidDactylorhiza sambucina commonly produces yellow-flowered and purple-flowered individuals in frequencies that range from balanced (per population) to very unbalanced, with parts of the species’ range entirely monochromatic. We studied male and female reproductive success of the two morphs in 22 populations in the Czech Republic, relating it to morph frequency, population size and density, and presence and abundance of yellow and purple co-flowering nectar-providing species visited by the same bee species. Cumulative abundances of yellow nectar-producing co-flowering species (of which, on average,Primula veris made up 56%) had a negative effect on male reproductive success of the yellow morph, and spectral analyses showed that to bumblebees the colours ofP. veris and yellowD. sambucina are different, permitting ready visual discrimination. The cumulative abundance of purple co-flowering species had no significant effect on morph reproductive success. Morph frequencies were unrelated to reproductive success and population size, and there was no evidence of frequency-dependent selection except in one highly unbalanced population. Density of flowering conspecifics was negatively correlated with male reproductive success of the purple morph. Seed mass, viability, and germination success depended on whether seeds resulted from outcrossed or selfed matings and on morph colour. Selfed seeds and seeds produced by the yellow morph from yellow × yellow and yellow × purple crosses had zero germination (after three months), providing the first hint that differential vegetative fitness, rather than differential reproductive fitness via pollinator selection, may explain morph frequencies inD. sambucina.     

Fitness consequences of redundant cues of competition in male Drosophila melanogaster

Phenotypic plasticity can allow animals to adapt their behavior, such as their mating effort, to their social and sexual environment. However, this relies on the individual receiving accurate and reliable cues of the environmental conditions. This can be achieved via the receipt of multimodal cues, which may provide redundancy and robustness. Male Drosophila melanogaster detect presence of rivals via combinations of any two or more redundant cue components (sound, smell, and touch) and respond by extending their subsequent mating duration, which is associated with higher reproductive success. Although alternative combinations of cues of rival presence have previously been found to elicit equivalent increases in mating duration and offspring production, their redundancy in securing success under sperm competition has not previously been tested. Here, we explicitly test this by exposing male D. melanogaster to alternative combinations of rival cues, and examine reproductive success in both the presence and absence of sperm competition. The results supported previous findings of redundancy of cues in terms of behavioral responses. However, there was no evidence of reproductive benefits accrued by extending mating duration in response to rivals. The lack of identifiable fitness benefits of longer mating under these conditions, both in the presence and absence of sperm competition, contrasted with some previous results, but could be explained by (a) damage sustained from aggressive interactions with rivals leading to reduced ability to increase ejaculate investment, (b) presence of features of the social environment, such as male and female mating status, that obscured the fitness benefits of longer mating, and (c) decoupling of behavioral investment with fitness benefits.     

Information content of female copulation calls in yellow baboons.

In a wide variety of animal species, females produce vocalizations just before, during, or immediately after copulation. Observational and experimental evidence indicates that these copulation calls are sexually selected traits, functioning to promote competition between males for access to the calling female. In this paper, we present an acoustic analysis of variation in the form of copulation calls of female yellow baboons, Papio cynocephalus cynocephalus. In particular, we examine whether information about three factors-the calling female's reproductive state, the occurrence or absence of ejaculation, and the dominance rank of the mating male-is encoded in call structure and hence is potentially available to male receivers attending to the signal. Although several features of copulation calls were correlated with each of these factors, when all three were included in multiple regressions only reproductive state and rank of the mating male had independent effects on call form. These findings indicate that female copulation calls in this species signal information about the proximity to ovulation of the calling female and also the relative competitive strength of her mating partner.     

Sounds different: inbreeding depression in sexually selected traits in the cricket Teleogryllus commodus

If male sexual signalling is honest because it captures genetic variation in condition then traits that are important mate choice cues should be disproportionately affected by inbreeding relative to other traits. To test this, we investigated the effect of brother-sister mating on advertisement calling by male field crickets Teleogryllus commodus. We quantified the effect of one generation of inbreeding on nightly calling effort and five finer-scale aspects of call structure that have been shown to influence attractiveness. We also quantified inbreeding depression on six life history traits and one morphological trait. Inbreeding significantly reduced hatching success, nymph survival and adult lifespan but had no detectable effect on hatching rate, developmental rate or adult body mass. The effect of inbreeding on sexually selected traits was equivocal. There was no decline in calling effort (seconds of sound production/night) by inbred males, but there were highly significant changes in three of five finer-scale call parameters. Sexually selected traits clearly vary in their susceptibility to inbreeding depression.     

Condition-dependent reproductive effort in frogs infected by a widespread pathogen

To minimize the negative effects of an infection on fitness, hosts can respond adaptively by altering their reproductive effort or by adjusting their timing of reproduction. We studied effects of the pathogenic fungus Batrachochytrium dendrobatidis on the probability of calling in a stream-breeding rainforest frog (Litoria rheocola). In uninfected frogs, calling probability was relatively constant across seasons and body conditions, but in infected frogs, calling probability differed among seasons (lowest in winter, highest in summer) and was strongly and positively related to body condition. Infected frogs in poor condition were up to 40% less likely to call than uninfected frogs, whereas infected frogs in good condition were up to 30% more likely to call than uninfected frogs. Our results suggest that frogs employed a pre-existing, plastic, life-history strategy in response to infection, which may have complex evolutionary implications. If infected males in good condition reproduce at rates equal to or greater than those of uninfected males, selection on factors affecting disease susceptibility may be minimal. However, because reproductive effort in infected males is positively related to body condition, there may be selection on mechanisms that limit the negative effects of infections on hosts.     

Biological invasions and the acoustic niche: the effect of bullfrog calls on the acoustic signals of white-banded tree frogs

Invasive species are known to affect native species in a variety of ways, but the effect of acoustic invaders has not been examined previously. We simulated an invasion of the acoustic niche by exposing calling native male white-banded tree frogs (Hypsiboas albomarginatus) to recorded invasive American bullfrog (Lithobates catesbeianus) calls. In response, tree frogs immediately shifted calls to significantly higher frequencies. In the post-stimulus period, they continued to use higher frequencies while also decreasing signal duration. Acoustic signals are the primary basis of mate selection in many anurans, suggesting that such changes could negatively affect the reproductive success of native species. The effects of bullfrog vocalizations on acoustic communities are expected to be especially severe due to their broad frequency band, which masks the calls of multiple species simultaneously.     

A reconciliation of inclusive fitness and personal fitness approaches: a proposed correcting term for the inclusive fitness formula

Hamilton implicitly defined the inclusive fitness of an individual as the number of genomes, identical by descent to its own, but not in its own body, which owe their existence to expression of genes in said individual. Hamilton regarded inclusive fitness as the true metric of evolutionary success and the thin- maximized by selection. Williams, Stern and Orlove either claimed this property for mean reproductive success, or stated that expected reproductive success equals expected inclusive fitness. These statements are reconciled if a correcting term is added to Hamilton's inclusive fitness formula.This change completely accounts for inclusive fitness in personal fitness terminology. The use of ? in place of r renders the new formula exact. This has less numerical impact than the addition of the correcting term to begin with, but helps show inclusive fitness theory holds exactly.     

Multimodal cues improve prey localization under complex environmental conditions

Predators often eavesdrop on sexual displays of their prey. These displays can provide multimodal cues that aid predators, but the benefits in attending to them should depend on the environmental sensory conditions under which they forage. We assessed whether bats hunting for frogs use multimodal cues to locate their prey and whether their use varies with ambient conditions. We used a robotic set-up mimicking the sexual display of a male túngara frog (Physalaemus pustulosus) to test prey assessment by fringe-lipped bats (Trachops cirrhosus). These predatory bats primarily use sound of the frog''s call to find their prey, but the bats also use echolocation cues returning from the frog''s dynamically moving vocal sac. In the first experiment, we show that multimodal cues affect attack behaviour: bats made narrower flank attack angles on multimodal trials compared with unimodal trials during which they could only rely on the sound of the frog. In the second experiment, we explored the bat''s use of prey cues in an acoustically more complex environment. Túngara frogs often form mixed-species choruses with other frogs, including the hourglass frog (Dendropsophus ebraccatus). Using a multi-speaker set-up, we tested bat approaches and attacks on the robofrog under three different levels of acoustic complexity: no calling D. ebraccatus males, two calling D. ebraccatus males and five D. ebraccatus males. We found that bats are more directional in their approach to the robofrog when more D. ebraccatus males were calling. Thus, bats seemed to benefit more from multimodal cues when confronted with increased levels of acoustic complexity in their foraging environments. Our data have important consequences for our understanding of the evolution of multimodal sexual displays as they reveal how environmental conditions can alter the natural selection pressures acting on them.     

High Corticosterone,Not High Energy Cost,Correlates with Reproductive Success in the Burrow-Nesting Ancient Murrelet

Theory and observations suggest that offspring abandonment in animals may occur when the costs to future reproductive output of current reproductive effort outweigh the fitness benefits of rearing the current brood. While hormonal cues (i.e. corticosterone) or energy reserves are believed to be involved, few studies have directly focused on the proximate cues influencing behaviours directly related to reproductive success. To address this information gap, we determined the incubation metabolic rates and corticosterone (CORT) levels of naturally fasting and freely incubating ancient murrelets (Synthliboramphus antiquus). Respiratory quotient (RQ) increased with date, suggesting that incubating ancient murrelets shifted from strictly lipid-based metabolism towards more protein-based metabolism as incubation progressed. Birds that hatched only one nestling had higher levels of circulating CORT than those which hatched two, suggesting that birds which laid only a single egg found incubation more stressful than those which laid two. However, CORT levels and incubation shift lengths were not correlated, suggesting that birds that undertook prolonged incubation shifts did so only when their energy stores were not jeopardized.     

An experimental investigation into status-dependent male dimorphism in the European earwig, Forficula auricularia

Discrete alternative reproductive phenotypes are probably often due to individuals adopting alternative tactics with unequal fitnesses in conditional strategies with status-dependent selection. One tactic is believed to be favoured below a status switch point and another tactic above it, owing to different fitness functions of the tactics. Males of the European earwig are dimorphic. Macrolabic males are large (high status) and have long forceps, and brachylabic males are small (low status) with short forceps. I tested whether fitness functions, measured as mating success, of the two morphs differed with regard to forceps length and body weight. Macrolabic males with longer forceps than a competing male had higher mating success but brachylabic males benefited by being heavier than their competitor. Thus, different selection regimes were acting on the two morphs, suggesting that their fitness functions differed in relation to status. These observations and those of previous studies, showing that morph expression is environmentally determined and is associated with body size and that the morphs have unequal fitness, provide support for the hypothesis that male dimorphism in this species is a conditional strategy that has evolved under status-dependent selection. The differential investment in forceps growth that characterizes the morphs was manifested in a steeper allometric relation between forceps length and body size in macrolabic than brachylabic males. Behavioural observations showed that males of both morphs engaged in direct contests for females. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Hybridization rapidly reduces fitness of a native trout in the wild

Human-mediated hybridization is a leading cause of biodiversity loss worldwide. How hybridization affects fitness and what level of hybridization is permissible pose difficult conservation questions with little empirical information to guide policy and management decisions. This is particularly true for salmonids, where widespread introgression among non-native and native taxa has often created hybrid swarms over extensive geographical areas resulting in genomic extinction. Here, we used parentage analysis with multilocus microsatellite markers to measure how varying levels of genetic introgression with non-native rainbow trout (Oncorhynchus mykiss) affect reproductive success (number of offspring per adult) of native westslope cutthroat trout (Oncorhynchus clarkii lewisi) in the wild. Small amounts of hybridization markedly reduced fitness of male and female trout, with reproductive success sharply declining by approximately 50 per cent, with only 20 per cent admixture. Despite apparent fitness costs, our data suggest that hybridization may spread due to relatively high reproductive success of first-generation hybrids and high reproductive success of a few males with high levels of admixture. This outbreeding depression suggests that even low levels of admixture may have negative effects on fitness in the wild and that policies protecting hybridized populations may need reconsideration.