QTL analysis of a rapidly evolving speciation phenotype in the Hawaiian cricket Laupala

In mate recognition systems, the functional necessity to coordinate traits involved in sexual communication should result in reduced pairing potential for new variants outside the distribution of common reproductive signals. Yet, many closely related, sexual species differ in mate recognition traits, suggesting that directional selection influences the divergence of mate recognition systems. Species of the endemic Hawaiian cricket genus Laupala are morphologically and ecologically cryptic, although both male calling song and female acoustic preference have diverged rapidly between closely related species. These mate recognition phenotypes are therefore often likely to be speciation phenotypes, i.e. traits whose divergence contributes, directly or indirectly, to a reduction of gene flow during speciation, given their frequent participation in early lineage divergence. We conducted a replicated, quantitative trait loci (QTL) mapping study of the genetic basis of differences in male calling song between two closely related species, Laupala paranigra and Laupala kohalensis, allowing us to examine the genetic basis of traits involved in rapid speciation. We found statistical support for eight QTL in one replicate, with at least four of these QTL mapping to the same regions in a second replicate. QTL effects ranged between 3.0% and 10.7% of the difference in pulse rate between L. paranigra and L. kohalensis, and are thus of moderate to small effect. All QTL identified show directional effects consistent with the hypothesis of directional selection. Thus, we conclude that rapid speciation can occur under the influence of many genes of moderate to small effect. This study implicates the role of directional selection in the divergence of mate recognition traits and speciation the Hawaiian cricket genus Laupala.     

Conserved visual sensitivities across divergent lizard lineages that differ in an ultraviolet sexual signal

The sensory drive hypothesis predicts the correlated evolution of signaling traits and sensory perception in differing environments. For visual signals, adaptive divergence in both color signals and visual sensitivities between populations may contribute to reproductive isolation and promote speciation, but this has rarely been tested or shown in terrestrial species. We tested whether opsin protein expression differs between divergent lineages of the tawny dragon (Ctenophorus decresii) that differ in the presence/absence of an ultraviolet sexual signal. We measured the expression of four retinal cone opsin genes (SWS1, SWS2, RH2, and LWS) using droplet digital PCR. We show that gene expression between lineages does not differ significantly, including the UV wavelength sensitive SWS1. We discuss these results in the context of mounting evidence that visual sensitivities are highly conserved in terrestrial systems. Multiple competing requirements may constrain divergence of visual sensitivities in response to sexual signals. Instead, signal contrast could be increased via alternative mechanisms, such as background selection. Our results contribute to a growing understanding of the roles of visual ecology, phylogeny, and behavior on visual system evolution in reptiles.     

Testing sensory drive speciation in cichlid fish: Linking light conditions to opsin expression,opsin genotype and female mate preference

Ecological speciation is facilitated when divergent adaptation has direct effects on selective mating. Divergent sensory adaptation could generate such direct effects, by mediating both ecological performance and mate selection. In aquatic environments, light attenuation creates distinct photic environments, generating divergent selection on visual systems. Consequently, divergent sensory drive has been implicated in the diversification of several fish species. Here, we experimentally test whether divergent visual adaptation explains the divergence of mate preferences in Haplochromine cichlids. Blue and red Pundamilia co‐occur across south‐eastern Lake Victoria. They inhabit different photic conditions and have distinct visual system properties. Previously, we documented that rearing fish under different light conditions influences female preference for blue versus red males. Here, we examine to what extent variation in female mate preference can be explained by variation in visual system properties, testing the causal link between visual perception and preference. We find that our experimental light manipulations influence opsin expression, suggesting a potential role for phenotypic plasticity in optimizing visual performance. However, variation in opsin expression does not explain species differences in female preference. Instead, female preference covaries with allelic variation in the long‐wavelength‐sensitive opsin gene (LWS), when assessed under broad‐spectrum light. Taken together, our study presents evidence for environmental plasticity in opsin expression and confirms the important role of colour perception in shaping female mate preferences in Pundamilia. However, it does not constitute unequivocal evidence for the direct effects of visual adaptation on assortative mating.     

Female Mate Choice Can Drive the Evolution of High Frequency Echolocation in Bats: A Case Study with Rhinolophus mehelyi

Animals employ an array of signals (i.e. visual, acoustic, olfactory) for communication. Natural selection favours signals, receptors, and signalling behaviour that optimise the received signal relative to background noise. When the signal is used for more than one function, antagonisms amongst the different signalling functions may constrain the optimisation of the signal for any one function. Sexual selection through mate choice can strongly modify the effects of natural selection on signalling systems ultimately causing maladaptive signals to evolve. Echolocating bats represent a fascinating group in which to study the evolution of signalling systems as unlike bird songs or frog calls, echolocation has a dual role in foraging and communication. The function of bat echolocation is to generate echoes that the calling bat uses for orientation and food detection with call characteristics being directly related to the exploitation of particular ecological niches. Therefore, it is commonly assumed that echolocation has been shaped by ecology via natural selection. Here we demonstrate for the first time using a novel combined behavioural, ecological and genetic approach that in a bat species, Rhinolophus mehelyi: (1) echolocation peak frequency is an honest signal of body size; (2) females preferentially select males with high frequency calls during the mating season; (3) high frequency males sire more off-spring, providing evidence that echolocation calls may play a role in female mate choice. Our data refute the sole role of ecology in the evolution of echolocation and highlight the antagonistic interplay between natural and sexual selection in shaping acoustic signals.     

Candidate neural locus for sex differences in reproductive decisions

Sexual selection and signal detection theories predict that females should be selective in their responses to mating signals in mate choice, while the response of males to signals in male competition should be less selective. The neural processes underlying this behavioural sex difference remain obscure. Differences in behavioural selectivity could result from differences in how sensitive sensory systems are to mating signals, distinct thresholds in motor areas regulating behaviour, or sex differences in selectivity at a gateway relaying sensory information to motor systems. We tested these hypotheses in frogs using the expression of egr-1 to quantify the neural responses of each sex to mating signals. We found that egr-1 expression in a midbrain auditory region was elevated in males in response to both conspecific and heterospecific calls, whereas in females, egr-1 induction occurred only in response to conspecific signals. This differential neural selectivity mirrored the sex differences in behavioural responsiveness to these stimuli. By contrast, egr-1 expression in lower brainstem auditory centres was not different in males and females. Our results support a model in which sex differences in behavioural selectivity arise from sex differences in the neural selectivity in midbrain areas relaying sensory information to the forebrain.     

Investment in attending to cues and the evolution of amplifiers

Signals and cues are extensively used in social interactions across diverse communication systems. Here, we extend an existing theoretical framework to explore investment by emitters and perceivers in the fidelity with which cues and signals associated with the former are detected by the latter. Traits of the emitter that improve cue or signal fidelity without adding information are termed ‘amplifiers’. We assume that each party can invest in improving fidelity but that it is increasingly costly the more fidelity is improved. Our model predicts that evolution of amplifier traits of a pre‐existing cue occurs over a broader range of circumstances than evolution of signalling in situations where the emitter offered no pre‐existing cue to the perceiver. It further predicts that the greater the intrinsic informational value of a cue, the more likely it is that the perceiver (and not the emitter) will invest in the fidelity of detecting that cue. A consequence of this predicted asymmetry is that true communication with reciprocal adaptations in emitters and perceivers to improve signal fidelity is likely to occur predominantly for traits of intermediate reliability. The corollary is that uncertainty of the perceiver will then be a key feature of communication. Uncertainty can arise because perceivers misinterpret signals or do not perceive them correctly, but here we argue that uncertainty is more fundamentally at the root of communication because traits that are intrinsically highly informative will induce only the perceiver and not the emitter to invest in improved fidelity of perception of that trait.     

Mate location, antennal morphology, and ecology in two praying mantids (Insecta: Mantodea)

The sensory systems employed by animals to locate potential mates are diverse. Among insects, chemical and acoustic signals are commonly used over long distances, with visual signals playing a role in close-range orientation and courtship. Within groups that exhibit a scramble competition mating system, selection on mate searching ability will be particularly strong. Clearly, aspects of the species ecology, such as habitat complexity and population density, will be crucial in the evolution of mate searching systems and sexual signals. Praying mantids exhibit both chemical and visual sexual signalling behaviour, and also vary in their ecology. This study employs scanning electron microscopy of antennal sensory morphology and behavioural assays to investigate the relative importance of chemical and visual signalling in two Australian praying mantid species: Pseudomantis albofimbriata and Ciulfina biseriata . As predicted, the high level of habitat complexity, low population density and strong male dispersal capability of P. albofimbriata corresponded to the use of airborne sex pheromones. Conversely, the open habitat, high population density, and poor dispersal of C. biseriata corresponded to a greater reliance on short-range visual cues for mate location.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 307–313.     

Divergence in Female Duetting Signals in the Enchenopa binotata Species Complex of Treehoppers (Hemiptera: Membracidae)

Sexual communication often involves signal exchanges between the sexes, or duetting, in which mate choice is expressed through response signals. With both sexes acting as signalers and receivers, variation in the signals of males and females may be important for mate choice, reproductive isolation, and divergence. In the Enchenopa binotata species complex – a case study of sympatric speciation in which vibrational duetting may have an important role – male signals are species‐specific, females choose among males on the basis of signal traits that reflect species and individual differences, and female preferences have exerted divergent selection on male signals. Here, we describe variation in female signals in the E. binotata species complex. We report substantial species differences in the spectral and temporal features of female signals, and in their timing relative to male signals. These differences were similar in range to differences in male signals in the E. binotata complex. We consider processes that might contribute to divergence in female signals, and suggest that signal evolution in the E. binotata complex may be influenced by mate choice in both sexes.     

Communication in troubled waters: responses of fish communication systems to changing environments

Fish populations are increasingly being subjected to anthropogenic changes to their sensory environments. The impact of these changes on inter- and intra-specific communication, and its evolutionary consequences, has only recently started to receive research attention. A disruption of the sensory environment is likely to impact communication, especially with respect to reproductive interactions that help to maintain species boundaries. Aquatic ecosystems around the world are being threatened by a variety of environmental stressors, causing dramatic losses of biodiversity and bringing urgency to the need to understand how fish respond to rapid environmental changes. Here, we discuss current research on different communication systems (visual, chemical, acoustic, electric) and explore the state of our knowledge of how complex systems respond to environmental stressors using fish as a model. By far the bulk of our understanding comes from research on visual communication in the context of mate selection and competition for mates, while work on other communication systems is accumulating. In particular, it is increasingly acknowledged that environmental effects on one mode of communication may trigger compensation through other modalities. The strength and direction of selection on communication traits may vary if such compensation occurs. However, we find a dearth of studies that have taken a multimodal approach to investigating the evolutionary impact of environmental change on communication in fish. Future research should focus on the interaction between different modes of communication, especially under changing environmental conditions. Further, we see an urgent need for a better understanding of the evolutionary consequences of changes in communication systems on fish diversity.     

Aposematism increases acoustic diversification and speciation in poison frogs

Multimodal signals facilitate communication with conspecifics during courtship, but they can also alert eavesdropper predators. Hence, signallers face two pressures: enticing partners to mate and avoiding detection by enemies. Undefended organisms with limited escape abilities are expected to minimize predator recognition over mate attraction by limiting or modifying their signalling. Alternatively, organisms with anti-predator mechanisms such as aposematism (i.e. unprofitability signalled by warning cues) might elaborate mating signals as a consequence of reduced predation. We hypothesize that calls diversified in association with aposematism. To test this, we assembled a large acoustic signal database for a diurnal lineage of aposematic and cryptic/non-defended taxa, the poison frogs. First, we showed that aposematic and non-aposematic species share similar extinction rates, and aposematic lineages diversify more and rarely revert to the non-aposematic phenotype. We then characterized mating calls based on morphological (spectral), behavioural/physiological (temporal) and environmental traits. Of these, only spectral and temporal features were associated with aposematism. We propose that with the evolution of anti-predator defences, reduced predation facilitated the diversification of vocal signals, which then became elaborated or showy via sexual selection.     

Developmental effects of visual environment on species‐assortative mating preferences in Lake Victoria cichlid fish

Local adaptation can be a potent force in speciation, with environmental heterogeneity leading to niche specialization and population divergence. However, local adaption often requires nonrandom mating to generate reproductive isolation. Population divergence in sensory properties can be particularly consequential in speciation, affecting both ecological adaptation and sexual communication. Pundamilia pundamila and Pundamilia nyererei are two closely related African cichlid species that differ in male coloration, blue vs. red. They co‐occur at rocky islands in southern Lake Victoria, but inhabit different depth ranges with different light environments. The species differ in colour vision properties, and females exert species‐specific preferences for blue vs. red males. Here, we investigated the mechanistic link between colour vision and preference, which could provide a rapid route to reproductive isolation. We tested the behavioural components of this link by experimentally manipulating colour perception – we raised both species and their hybrids under light conditions mimicking shallow and deep habitats – and tested female preference for blue and red males under both conditions. We found that rearing light significantly affected female preference: shallow‐reared females responded more strongly to P. pundamilia males and deep‐reared females favoured P. nyererei males – implying that visual development causally affects mate choice. These results are consistent with sensory drive predictions, suggesting that the visual environment is key to behavioural isolation of these species. However, the observed plasticity could also make the species barrier vulnerable to environmental change: species‐assortative preferences were weaker in females that were reared in the other species’ light condition.     

Host shifts and signal divergence: mating signals covary with host use in a complex of specialized plant‐feeding insects

A combination of divergent natural and sexual selection is a powerful cause of speciation. This conjunction of evolutionary forces may often occur when divergence is initiated by ecological differences between populations because local adaptation to new resources can lead to changes in sexual selection. The hypothesis that differences in resource use contribute to the evolution of reproductive isolation by altering the nature of sexual selection predicts that: (1) differences in sexual traits, such as signals and preferences, are an important source of reproductive isolation between species using different resources; (2) there are identifiable sources of selection on sexual traits that differ between species using different resources; and (3) signals vary between populations using different resources to a larger extent than between populations using the same resource at different localities. Testing these predictions requires a group of closely‐related species or populations that specialize on different resources and for which the traits involved in mate choice are known. The Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae) are host plant specialists in which speciation is associated with shifts to novel host plants. Mating in this complex is preceded by an exchange of vibrational signals transmitted through host plant stems, and the signal traits important for mate choice have been identified. In the E. binotata complex, previous work has supported the first two predictions: (1) signal differences between species are important in mate recognition and (2) host shifts can alter both the trait values favoured by sexual selection and the evolutionary response to that selection. In the present study, we tested the last prediction by conducting a large‐scale study of mating signal variation within and between the 11 species in the complex. We find that differences in host use are strongly associated with differences in signal traits important for mate recognition. This result supports the hypothesis that hosts shifts have led to speciation in this group in part through their influence on divergence in mate communication systems. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 60–72.     

Selection on male sex pheromone composition contributes to butterfly reproductive isolation

Selection can facilitate diversification by inducing character displacement in mate choice traits that reduce the probability of maladaptive mating between lineages. Although reproductive character displacement (RCD) has been demonstrated in two-taxa case studies, the frequency of this process in nature is still debated. Moreover, studies have focused primarily on visual and acoustic traits, despite the fact that chemical communication is probably the most common means of species recognition. Here, we showed in a large, mostly sympatric, butterfly genus, a strong pattern of recurrent RCD for predicted male sex pheromone composition, but not for visual mate choice traits. Our results suggest that RCD is not anecdotal, and that selection for divergence in male sex pheromone composition contributed to reproductive isolation within the Bicyclus genus. We propose that selection may target olfactory mate choice traits as a more common sensory modality to ensure reproductive isolation among diverging lineages than previously envisaged.     

How sensory drive can promote speciation

Some of the most spectacular and diverse traits in animals are the signals used to attract mates. Closely related species often differ dramatically in signaling traits, in spite of similarity in other morphological traits. The idea that reproductive isolation arises when male mating signals and female preferences differ among populations is an old one. However, until recently, there was almost no information on what generates diversity in mating signals and preferences. This is beginning to change, with emerging results that highlight the importance of habitat differences in generating this diversity. Such differences in ecology are at the root of one hypothesis for divergence in sexual signaling – sensory drive. The sensory drive hypothesis focuses on how communication systems adapt to local environments and predicts that divergence in communication systems will occur when environments differ. Reproductive isolation can arise as a byproduct of this adaptive divergence in behavior.     

Sensory trade-offs predict signal divergence in Surfperch

Unidirectional elaboration of male trait evolution (e.g., larger, brighter males) has been predicted by receiver bias models of sexual selection and empirically tested in a number of different taxa. This study identifies a bidirectional pattern of male trait evolution and suggests that a sensory constraint is driving this divergence. In this system, the inherent trade-off in dichromatic visual detection places limits on the direction that sensory biases may take and thus provides a quantitative test of the sensory drive model. Here I show that sensory systems with trade-offs in detection abilities produce bidirectional biases and that signal design properties match these biases. I combine species-specific measurements and ancestral estimates with visual detection modeling to examine biases in sensory and signaling traits across five fish species occupying optically diverse habitats in the Californian kelp forest. Species-specific divergence in visual pigments correlates with changes in environment and produces different sensory biases--favoring luminance (brightness) detection for some species and chromatic (color) detection for others. Divergence in male signals (spectral reflectance of orange, blue, and silver color elements) is predicted by each species' sensory bias: color divergence favors chromatic detection for species with chromatically biased visual systems, whereas species with luminance sensory biases have signals favoring luminance detection. This quantitative example of coevolution of communication traits varying in a bidirectional pattern governed by the environment is the first demonstration of sensory trade-offs driving signal evolution.     

Sensory‐based conservation of seabirds: a review of management strategies and animal behaviours that facilitate success

Sensory‐based conservation harnesses species' natural communication and signalling behaviours to mitigate threats to wild populations. To evaluate this emerging field, we assess how sensory‐based manipulations, sensory mode, and target taxa affect success. To facilitate broader, cross‐species application of successful techniques, we test which behavioural and life‐history traits correlate with positive conservation outcomes. We focus on seabirds, one of the world's most rapidly declining groups, whose philopatry, activity patterns, foraging, mate choice, and parental care behaviours all involve reliance on, and therefore strong selection for, sophisticated sensory physiology and accurate assessment of intra‐ and inter‐species signals and cues in several sensory modes. We review the use of auditory, olfactory, and visual methods, especially for attracting seabirds to newly restored habitat or deterring birds from fishing boats and equipment. We found that more sensory‐based conservation has been attempted with Procellariiformes (tube‐nosed seabirds) and Charadriiformes (e.g. terns and gulls) than other orders, and that successful outcomes are more likely for Procellariiformes. Evolutionary and behavioural traits are likely to facilitate sensory‐based techniques, such as social attraction to suitable habitat, across seabird species. More broadly, successful application of sensory‐based conservation to other at‐risk animal groups is likely to be associated with these behavioural and life‐history traits: coloniality, philopatry, nocturnal, migratory, long‐distance foraging, parental care, and pair bonds/monogamy.     

THE IMPORTANCE OF FEMALE CHOICE,MALE–MALE COMPETITION,AND SIGNAL TRANSMISSION AS CAUSES OF SELECTION ON MALE MATING SIGNALS

Selection on advertisement signals arises from interacting sources including female choice, male–male competition, and the communication channel (i.e., the signaling environment). To identify the contribution of individual sources of selection, we used previously quantified relationships between signal traits and each putative source to predict relationships between signal variation and fitness in Enchenopa binotata treehoppers (Hemiptera: Membracidae). We then measured phenotypic selection on signals and compared predicted and realized relationships between signal traits and mating success. We recorded male signals, then measured lifetime mating success at two population densities in a realistic environment in which sources of selection could interact. We identified which sources best predicted the relationship between signal variation and mating success using a multiple regression approach. All signal traits were under selection in at least one of the two breeding seasons measured, and in some cases selection was variable between years. Female preference was the strongest source of selection shaping male signals. The E. binotata species complex is a model of ecological speciation initiated by host shifts. Signal and preference divergence contribute to behavioral isolation within the complex, and the finding that female mate preferences drive signal evolution suggests that speciation in this group results from both ecological divergence and sexual selection.     

From Sender to Receiver: Propagation and Environmental Effects on Acoustic Signals

SYNOPSIS. Acoustic signals transmitted over large distancesdiffer significantly from those emitted by the signaler. Acousticsignals degrade in amplitude, spectral and temporal structureas they propagate through theenvironment. A great deal of workon acoustic communication is aimed at understanding the selectiveforces imposed by the environment on animal signals. I willdiscuss the physical constraints the environment puts on acousticcommunication, and then discuss similarities in communicationby anurans and insects that relate these environmental constraintsto their signaling systems. Lastly, I show how changes in signalsduring propagation relate to changes in signal perception duringphonotaxis, and thus, how propagation relates to mate choiceand sexual selection     

Reproductive interference via display signals: the challenge of multiple receivers

Sexually selected traits important in both mate and competitor recognition provide an opportunity to understand the tradeoffs associated with reproductive and competitive interference. When co-occurring species compete over similar resources, selection may promote signal similarity to facilitate competitive interactions in opposition to selection for signal divergence to maintain assortative mating. Bird song provides a classic example of contrasting selection on signal design, because songs function both in mate discrimination and in territorial advertisement. Similarity in songs aids competitor recognition both within and across species, and song convergence or mixing is widespread in the songbirds. Two related mechanisms can maintain mate recognition in the face of song convergence. First, multiple recognition signals, both across and within signaling modalities, provide a basis for mate and competitor discrimination using different sets of cues. Second, stricter female song preferences may allow interspecific male–male competitive communication without compromising female mate discrimination. I suggest that increased understanding of the neurobiology underlying song recognition will provide insight into the relative importance and prevalence of these different mechanisms along a continuum of species divergence.     

Wax,sex and the origin of species: Dual roles of insect cuticular hydrocarbons in adaptation and mating

Evolutionary changes in traits that affect both ecological divergence and mating signals could lead to reproductive isolation and the formation of new species. Insect cuticular hydrocarbons (CHCs) are potential examples of such dual traits. They form a waxy layer on the cuticle of the insect to maintain water balance and prevent desiccation, while also acting as signaling molecules in mate recognition and chemical communication. Because the synthesis of these hydrocarbons in insect oenocytes occurs through a common biochemical pathway, natural or sexual selection on one role may affect the other. In this review, we explore how ecological divergence in insect CHCs can lead to divergence in mating signals and reproductive isolation. We suggest that the evolution of insect CHCs may be ripe models for understanding ecological speciation.