Signal Traits Research Articles

Pollinator-mediated isolation promotes coexistence of closely related food-deceptive orchids.

Identifying the factors that contribute to reproductive isolation among closely-related species is key for understanding the diversification of lineages. In this study, we investigate the strength of premating and postmating reproductive isolation barriers between Disa ferruginea and Disa gladioliflora, a pair of closely-related species, often found co-flowering in sympatry. Both species are non-rewarding and rely on mimicry of different rewarding model flowers for attraction of pollinators. We constructed abiotic niche models for different forms of each taxon to measure ecogeographic isolation. Using experimental arrays in sympatry, we recorded pollinator transitions to measure ethological isolation. We performed hand pollinations to measure postpollination isolation. We found strong, but not complete, premating isolation associated with abiotic niches and absolute ethological isolation based on pollinator preferences in sympatry. Pollinator preferences among the orchids could be explained largely by flower colour (orange in D. ferruginea and pink in D. gladioliflora) which matches that of the pollinator food plants. Post-mating barriers were weak as the species were found to be inter-fertile. Coexistence in the orchid species pair is due mainly to ethological reproductive isolation arising from flower colour differences resulting from mimicry of different rewarding plants. These results highlight the importance of signalling traits for ethological isolation of closely-related species with specialized pollination systems.

Patterns of a sexually selected trait are not predictable across urban and non-urban populations of a songbird, the dark-eyed junco

Urbanization can result in novel selective pressures that can cause phenotypic differences amongst urban-tolerant species across urban and non-urban habitats. Here, we compared the size of the white tail patch (“tail white”), a sexual signaling trait, in two urban populations of dark-eyed juncos in comparison to neighboring non-urban populations. Contrary to our expectations, urban phenotypes did not differ from local wildlands in San Diego and Los Angeles counties in similar directions. While the San Diego population showed lower tail white compared to its neighboring wildland population, the Los Angeles population did not. The tail white of the Los Angeles population was not statistically different from that of the San Diego population, suggesting that urban populations may share similar environmental conditions yet face different selective clines due to urbanization. There were, however, differences between wildland populations. Differences in evolutionary histories, environmental conditions, and selective pressures within and outside urban areas may affect how urbanization facilitates population differentiation, even across urban populations of the same species.

Nanoscale ultrastructures increase the visual conspicuousness of signalling traits in obligate cleaner shrimps.

Signal theory predicts organisms should evolve signals that are conspicuous to intended receivers in natural signalling environments. Cleaner shrimps remove ectoparasites from reef fish clients and many signal their intent to clean by whipping long, white antennae. As white is a reliably conspicuous colour in aquatic environments, we hypothesized that selection has acted to increase broad-spectrum antennal reflectance in cleaners. Using scanning electron microscopy, optical models and reflectance measurements, we found that the antennae in three obligate cleaner species from two families (Palaemonidae and Lysmatidae) had thick (∼6 µm) chitinous layers or densely packed high refractive index spheres (300-400 nm diameter), which models show increase reflectance (400-700 nm). Two facultative and non-cleaning species had no visible antennae ultrastructure beyond the chitinous exoskeleton. Antennae reflectance was significantly higher in obligate cleaners than in facultative and non-cleaning species. Our results suggest that some obligate cleaners may have evolved ultrastructures that increase the conspicuousness of their antennae as signals.

EffiMultiOrthoBearNet: An Efficient Lightweight Architecture for Bearing Fault Diagnosis

Amidst the advent of Industry 4.0 and the rapid advancements in smart manufacturing, the imperative for developing resource-efficient condition monitoring and fault prediction technologies tailored for industrial equipment in resource-limited settings has become increasingly evident. This study puts forward EffiMultiOrthoBearNet, an innovative, lightweight, deep learning model specifically designed for the accurate identification and classification of bearing faults. Central to EffiMultiOrthoBearNet’s architecture is the integration of multi-scale convolutional layers and orthogonal attention mechanisms—key innovations that significantly enhance the model’s performance. Leveraging advanced feature extraction capabilities, EffiMultiOrthoBearNet meticulously processes Continuous Wavelet Transform (CWT) images from the CWRU dataset, ensuring the precise delineation of essential bearing signal traits through its multi-scale and attention-enhanced mechanisms. Optimized for supreme operational efficiency in resource-deprived environments, EffiMultiOrthoBearNet achieves unmatched classification accuracy—up to 100% under ideal circumstances and consistently above 90% amidst significant noise and operational complexities. Demonstrating remarkable adaptability and efficiency, EffiMultiOrthoBearNet provides a pioneering and practical fault diagnosis solution for industrial machinery across a wide range of application scenarios, even under stringent resource limitations.

Rising above the noise: the influence of population dynamics on the evolution of acoustic signaling

Acoustic signaling is employed by many sexually reproducing species to select for mates and enhance fitness. However, signaling in dense populations can create an auditory background, or chorus, which may interfere with a signal receiver’s phonotactic selectivity, or the ability to distinguish individual signals. Feedback between the strength of an individual’s signal, phonotactic selectivity, and population size, may interact in complex ways to impact the evolution of signaling within a population, potentially leading to the emergence of silence. Here we formulate a general model that captures the dynamic feedback between individual acoustic signalers, phonotactic selectivity, and the population-level chorus to explore the eco-evolutionary dynamics of an acoustic trait within a population. We find that population dynamics have a significant influence on the evolutionary dynamics of the signaling trait, and that very sharp transitions separate conspicuous from silent populations. Our framework also reveals that increased phonotactic selectivity promotes the stability of signaling populations, and that transitions from signaling to silence are prone to hysteresis. We suggest that understanding the relationship between factors influencing population size, such as environmental productivity, as well as factors influencing phonotactic selectivity, such as anthropogenic noise, are central to understanding the complex mosaic of acoustically signaling and silent populations.

A late burst of colour evolution in a radiation of songbirds (Passeriformes: Parulidae) suggests secondary contact drives signal divergence.

Evolutionary radiations provide important insights into species diversification, which is especially true of adaptive radiations. New World wood warblers (Parulidae) are a family of small, insectivorous, forest-dwelling passerine birds, often considered an exemplar of adaptive radiation due to their rapid diversification followed by a slowdown. However, they deviate from the expectations of an adaptive radiation scenario due to the lack of conspicuous morphological and ecological differentiation. We fitted several macroevolutionary models to trait data in 105 species of wood warblers. We tested whether morphological traits underwent an early burst of evolution (suggesting adaptation to new ecological niches in adaptive radiations) and whether song and colour underwent a diversity-dependent acceleration of trait evolutionary rate (consistent with reproductive interference driving signal evolution). Morphology and song evolved gradually under stabilizing selection, suggesting niche conservatism, with morphology possibly acting as a constraint on song evolution. In contrast, many feather colour traits underwent a diversity-dependent burst of evolution occurring late in the clade's history. We suggest that a two-step process has led to the remarkable diversification of wood warblers. First, their early diversification probably proceeded by allopatric speciation. Second, feather colour divergence likely occurred during secondary contact after range expansion. This diversification of signalling traits might have facilitated species coexistence, in combination with behavioural niche partitioning. Wood warblers seem to present characteristics of both adaptive and non-adaptive radiations.

Complexity of the Male Perfume of Eulaema nigrita from Forest and Woody Physiognomies of the Brazilian Savanna: Is There a Relationship with Body Size and Wing Wear?

Male orchid bees collect volatile and semi-volatile compounds from the environment for storage and accumulation in specialized hind legs. Later, these compounds form a perfume blend used during courtship to lure conspecific females for mating. Male orchid bees perfume has been suggested to play an important role as a sexual signaling trait involved in pre-mating isolation of species, functioning as an indicator of male genetic quality. Eulaema nigrita Lepeletier (Apidae: Euglossini) is a common species in both forested and woody savanna (Cerrado stricto sensu) physiognomies of the Brazilian savanna biome. By identifying the chemical composition of male E. nigrita perfume, we tested for differences in the bouquet chemical profile in populations from remnants of seasonal semideciduous forest and woody savanna. In addition, we assessed the relation between perfume complexity and morphological traits associated with size and age of males. Our analysis showed a low effect of physiognomies on differences in the perfume chemical profile of sampled males. Nevertheless, we observed significant differences in the chemical profile of individuals from two seasonal semideciduous forest remnants, which suggests an environmental effect in individual bouquet. Wing wear measurements were positively related to perfume complexity, consistent with the premise that perfumes from older individuals are indicators of survival capacity in male orchid bees.

Red fruits exhibit lower colour diversity than red flowers as perceived by birds

Abstract Pollination and seed dispersal are crucial processes for plant reproduction, sharing ecological relevance and similarities, yet they have rarely been considered together. Flowers appear to express greater phenotypic diversity than fruits due to multiple confounding factors, which pose challenges for comparative analyses. The colours of flowers and fruits are important visual signal traits in pollination and seed dispersal, evolving under different selective pressures from their respective pollinators and seed dispersers. Birds constitute a unique plant‐interacting group that participates in both pollination and seed dispersal events. In this study, we focus on red flowers and red fruits associated with avian mutualists to gain insight into the intrinsic differences between flowers/pollination and fruits/seed dispersal. We conducted comparisons of colouration between 94 red flowers pollinated by birds and 99 red fruits dispersed by birds. The colour diversity was compared in both the spectral space and the avian colour vision spaces. Colour conspicuousness was analysed using avian colour vision models, as well as bee models. Pigeon colour preference was tested by controlled experiments utilizing red stimuli with and without secondary peaks at short wavelengths. Red fruits had lower colour diversity than red flowers, with redder hues and fewer secondary reflectance peaks. Avian colour vision models illustrated that fruits were more conspicuous than flowers achromatically, but not chromatically. Pigeons did not show preference for red with or without a secondary peak. Although both are red, there are significant differences between flowers and fruits in terms of colour diversity, spectral properties and colour perceptions. As we exclusively considered avian mutualists, these differences cannot be attributed to the differences in interacting animal groups or to their colour vision properties. This implies that the differences in evolutionary history between flowers and fruits may deserve further attention to understand the colour evolution. Read the free Plain Language Summary for this article on the Journal blog.

High rates of male courtship in a female-ornamented pipefish.

In species with sex-specific signalling traits that appear to be ornamental (i.e. are conspicuous and with no obvious natural selection benefit), the ornamented sex typically initiates courtship and is most active in courtship. Here, we report for the first time courtship displays in the extremely sexually dimorphic, female-ornamented wide-bodied pipefish (Stigmatopora nigra), revealing unexpected behaviours. Females use their sex-specific ornament during courtship displays, as expected, but rarely in female-female interactions. Surprisingly, males initiated 61% of reciprocated courtship bouts and chased females in 17% of the bouts. This chasing behaviour could be a form of male harassment or be indicative of female disinterest in ardent males, either of which was unexpected to be found in this female-ornamented species. Our results highlight the need to study the details of species' behaviours in considering the potential roles of sexual selection and sexual conflict in shaping sexual dimorphism.

Stronger evidence for genetic ancestry than environmental conditions in shaping the evolution of a complex signalling trait during biological invasion.

Introductions of invasive species to new environments often result in rapid rates of trait evolution. While in some cases these evolutionary transitions are adaptive and driven by natural selection, they can also result from patterns of genetic and phenotypic variation associated with the invasion history. Here, we examined the brown anole (Anolis sagrei), a widespread invasive lizard for which genetic data have helped trace the sources of non-native populations. We focused on the dewlap, a complex signalling trait known to be subject to multiple selective pressures. We measured dewlap reflectance, pattern and size in 30 non-native populations across the southeastern United States. As well, we quantified environmental variables known to influence dewlap signal effectiveness, such as canopy openness. Further, we used genome-wide data to estimate genetic ancestry, perform association mapping and test for signatures of selection. We found that among-population variation in dewlap characteristics was best explained by genetic ancestry. This result was supported by genome-wide association mapping, which identified several ancestry-specific loci associated with dewlap traits. Despite the strong imprint of this aspect of the invasion history on dewlap variation, we also detected significant relationships between dewlap traits and local environmental conditions. However, we found limited evidence that dewlap-associated genetic variants have been subject to selection. Our study emphasizes the importance of genetic ancestry and admixture in shaping phenotypes during biological invasion, while leaving the role of selection unresolved, likely due to the polygenic genetic architecture of dewlaps and selection acting on many genes of small effect.

Honest floral signalling traits vary across and within populations in an insect‐pollinated plant

Abstract In flowering plants that produce concealed rewards, pollinator foraging preferences may select for floral advertisement traits that are correlated with rewards. To date, studies have not focused on the potential for honest signals to vary across populations, which could occur due to differences in pollinator communities or plant mating system. We tested for variation in honest signals across and within populations and mating systems in Arabis alpina, a broadly distributed arctic‐alpine perennial herb that is visited by a variable community of insects. In a greenhouse common garden, we tested for correlations between corolla area, floral scent and nectar volume in 29 populations. In 12 field populations, we examined variation in pollen limitation and corolla area. Across and within populations and mating systems, larger flowers generally produced more nectar. Total scent emission was not correlated with nectar production, but two compounds—phenylacetaldehyde and benzyl alcohol—may be honest signals in some populations. Corolla area was correlated with pollen limitation only across populations. Our results suggest that honest signals may be similar across populations but may not result from contemporary direct selection on floral advertisements. Read the free Plain Language Summary for this article on the Journal blog.

Signal size allometry in Anolis lizard dewlaps.

Positive allometry of signalling traits has often been taken as evidence for sexual selection. However, few studies have explored interspecific differences in allometric scaling relationships among closely related species that vary in their degree of ecological similarity. Anolis lizards possess an elaborate retractable throat fan called a dewlap that is used for visual communication and differs greatly in size and colour among species. We observed that Anolis dewlaps demonstrate positive allometry: relative dewlap size increases with body size. We also observed that coexisting species are divergent in signal size allometries, while convergent species-similar in other aspects of ecology, morphology and behaviour-typically share similar dewlap allometric scaling relationships. These patterns suggest that dewlap scaling relationships may follow the same pattern as other traits in the anole radiation, where ecologically different sympatric species have evolved a suite of divergent traits.

The optimal time to approach an unfamiliar object: a Bayesian model

Abstract Many organisms take time before approaching unfamiliar objects. This caution forms the basis of some well-known assays in the fields of behavioral ecology, comparative psychology, and animal welfare, including quantifying the personality traits of individuals and evaluating the extent of their neophobia. In this paper, we present a mathematical model which identifies the optimal time an observer should wait before approaching an unfamiliar object. The model is Bayesian, and simply assumes that the longer the observer goes without being attacked by an unfamiliar object, the lower will be the observer’s estimated probability that the object is dangerous. Given the information gained, a time is reached at which the expected benefits from approaching the object begin to exceed the costs. The model not only explains why latency to approach may be repeatable among individuals and varies with the object’s appearance but also why individuals habituate to the stimulus, approaching it more rapidly over repeated trials. We demonstrate the applicability of our model by fitting it to published data on the time taken by chicks to attack artificial caterpillars that share no, one, or two signaling traits with snakes (eyespots and posture). We use this example to show that while the optimal time to attack an unfamiliar object reflects the observer’s expectation that the object is dangerous, the rate at which habituation arises is also a function of the observer’s certainty in their belief. In so doing, we explain why observers become more rapidly habituated to “weaker” stimuli than the “stronger” ones.

Quantitative trait loci underlying a speciation phenotype.

Sexual signalling traits and their associated genetic components play a crucial role in the speciation process, as divergence in these traits can contribute to sexual isolation. Despite their importance, our understanding of the genetic basis of variable sexual signalling traits linked to speciation remains limited. In this study, we present new genetic evidence of Quantitative Trait Loci (QTL) underlying divergent sexual signalling behaviour, specifically pulse rate, in the Hawaiian cricket Laupala. By performing RNA sequencing on the brain and central nervous system of the parental species, we annotate these QTL regions and identify candidate genes associated with pulse rate. Our findings provide insights into the genetic processes driving reproductive isolation during speciation, with implications for understanding the mechanisms underlying species diversity.

When parents play favorites: brood demand shapes parental preference for offspring UV color.

Parents might initially produce more offspring than they might be able to raise. However, when offspring demand exceeds their parents´ rearing capacity, parents might shift care towards the offspring which yield greater fitness returns to achieve their optimal brood size via brood reduction. Such favoritism could rely on offspring signaling traits if these inform parents about offspring quality and hence about the pay-offs of their investment. Here we investigated whether favoritism of blue tit (Cyanistes caeruleus) parents for an offspring signal (i.e., ultraviolet (UV) plumage coloration) varies with brood demand. To test this, we experimentally blocked the UV reflectance of yellow breast feathers in half of the nestlings of each brood, and then we sequentially performed two opposing brood size manipulations to vary nestling demand below or above parental rearing capacity. In reduced broods, nestlings begged overall less intensely and gained more body mass, supporting that parental rearing capacities sufficed to satisfy brood demand. Moreover, in reduced broods, UV-blocked nestlings (i.e., low-quality offspring) were fed and prey-tested more often. Yet, they begged more than control nestlings, suggesting that they were perhaps treated differently by other family members or which they may exploit parental preferences beyond actual need (at least in reduced nests). Parents flexibly shifted their feeding rate and favoritism in response to short-term changes in family size, as there was no parental preference for enlarged broods. Such flexible parental feeding rules may allow parents to gain the upper hand in parent-offspring conflict. However, we did not find evidence that parental favoritism facilitated brood reduction, at least in conditions where demand was temporally enhanced.

An ultrasound absorbing inflorescence zone enhances echo-acoustic contrast of bat-pollinated cactus flowers.

Flowering plants have evolved an extraordinary variety of signaling traits to attract their pollinators. Most flowers rely on visual and chemical signals, but some bat-pollinated plants have evolved passive acoustic floral signals. All known acoustic flower signals rely on the same principle of increased sonar reflectivity. Here we describe a novel mechanism that relies on increased absorption of the area surrounding the flower. In a bat-pollinated cactus (Espostoa frutescens) we found a hairy inflorescence zone, a so called cephalium. Flowers solely emerge out of this zone. We measured the echoes of cephalia, flowers and unspecialized column surfaces and recorded echolocation calls of approaching bats. We found that the cephalium acts as strong ultrasound absorber, attenuating the sound by -14 dB. The absorption was highest around the echolocation call frequencies of approaching bats. Our results indicate that, instead of making flowers more reflective, plants can also evolve structures to attenuate the background echo, thereby enhancing the acoustic contrast with the target.

Haemosporidian parasites and incubation period influence plumage coloration in tanagers (Passeriformes: Thraupidae).

Birds are highly visually oriented and use plumage coloration as an important signalling trait in social communication. Hence, males and females may have different patterns of plumage coloration, a phenomenon known as sexual dichromatism. Because males tend to have more complex plumages, sexual dichromatism is usually attributed to female choice. However, plumage coloration is partly condition-dependent; therefore, other selective pressures affecting individuals' success may also drive the evolution of this trait. Here, we used tanagers as model organisms to study the relationships between dichromatism and plumage coloration complexity in tanagers with parasitism by haemosporidians, investment in reproduction and life-history traits. We screened blood samples from 2849 individual birds belonging to 52 tanager species to detect haemosporidian parasites. We used publicly available data for plumage coloration, bird phylogeny and life-history traits to run phylogenetic generalized least-square models of plumage dichromatism and complexity in male and female tanagers. We found that plumage dichromatism was more pronounced in bird species with a higher prevalence of haemosporidian parasites. Lastly, high plumage coloration complexity in female tanagers was associated with a longer incubation period. Our results indicate an association between haemosporidian parasites and plumage coloration suggesting that parasites impact mechanisms of sexual selection, increasing differences between the sexes, and social (non-sexual) selection, driving females to develop more complex coloration.

Female dewlap ornaments are evolutionarily labile and associated with increased diversification rates in Anolis lizards.

The evolution of costly signalling traits has largely focused on male ornaments. However, our understanding of ornament evolution is necessarily incomplete without investigating the causes and consequences of variation in female ornamentation. Here, we study the Anolis lizard dewlap, a trait extensively studied as a male secondary sexual characteristic but present in females of several species. We characterized female dewlaps for 339 species to test hypotheses about their evolution. Our results did not support the hypothesis that female dewlaps are selected against throughout the anole phylogeny. Rather, we found that female dewlaps were evolutionary labile. We also did not find support for the adaptive hypothesis that interspecific competition drove the evolution of female dewlaps. However, we did find support for the pleiotropy hypothesis as species with larger females and reduced sexual size dimorphism were more likely to possess female dewlaps. Lastly, we found that female dewlap presence influenced diversification rates in anoles, but only secondarily to a hidden state. Our results demonstrate that female ornamentation is widespread in anoles and the traditional hypothesis of divergent selection between the sexes does not fully explain their evolution. Instead, female ornamentation is likely to be subject to complex adaptive and non-adaptive evolutionary forces.

Increased Floral Rewards due to Local Adaptation Drives Plant Ecological Speciation via Learned Preferences of Pollinators.

AbstractIn animal-pollinated plants, the growth environment and pollination environment are two important agents of natural selection. However, their simultaneous effects on plant speciation remain underexplored. Here, we report a theoretical finding that if plants' local adaptation to the growth environment increases their floral rewards for pollinators, it can strongly facilitate ecological speciation in plants. We consider two evolving plant traits, vegetative and floral signal traits, in a population genetic model for two plant populations under divergent selection from different growth environments. The vegetative trait determines plants' local adaptation. Locally adapted plants reward pollinators better than maladapted plants. By associative learning, pollinators acquire learned preferences for floral signal traits expressed by better-rewarding plants. If pollinators' learned preferences become divergent between populations, floral signal divergence occurs and plants develop genetic associations between vegetative and floral signal traits, leading to ecological speciation via a two-allele mechanism. Interestingly, speciation is contingent on whether novel floral signal variants arise before or after plant populations become locally adapted to the growth environment. Our results suggest that simultaneous selection from growth and pollination environments might be important for the ecological speciation of animal-pollinated plants.

Sensory biases in response to novel complex acoustic signals in male and female grey treefrogs, Hyla chrysoscelis.

The sensory bias hypothesis proposes that female preferences for male sexual signalling traits evolved in contexts other than mating. Individuals of both sexes may experience similar selection pressures in these contexts; thus males may have similar biases to females for variation in signal traits. We tested this prediction in the grey treefrog, Hyla chrysoscelis, in which males produce simple advertisement calls, but females are more attracted to certain novel complex stimuli. We recorded males' responses to playbacks of both simple advertisement calls and complex calls consisting of the advertisement call with an acoustic appendage (filtered noise, or heterospecific call pulses) either leading or following the call. We tested females' preferences for the same stimuli in phonotaxis tests. We found evidence for a sensory bias in both sexes: males gave more aggressive calls in response to complex stimuli and females sometimes preferred complex over simple calls. These biases were not universal and depended on both temporal order and appendage characteristics, but how these effects manifested differed between the sexes. Ultimately, our approach of studying biases of both sexes in response to novel mating signals will shed light on the origin of mating preferences, and the mechanisms by which sensory biases operate.