Beauty in the eyes of the beholders: colour vision is tuned to mate preference in the Trinidadian guppy (Poecilia reticulata)

A broad range of animals use visual signals to assess potential mates, and the theory of sensory exploitation suggests variation in visual systems drives mate preference variation due to sensory bias. Trinidadian guppies (Poecilia reticulata), a classic system for studies of the evolution of female mate choice, provide a unique opportunity to test this theory by looking for covariation in visual tuning, light environment and mate preferences. Female preference co‐evolves with male coloration, such that guppy females from ‘low‐predation’ environments have stronger preferences for males with more orange/red coloration than do females from ‘high‐predation’ environments. Here, we show that colour vision also varies across populations, with ‘low’‐predation guppies investing more of their colour vision to detect red/orange coloration. In independently colonized watersheds, guppies expressed higher levels of both LWS‐1 and LWS‐3 (the most abundant LWS opsins) in ‘low‐predation’ populations than ‘high‐predation’ populations at a time that corresponds to differences in cone cell abundance. We also observed that the frequency of a coding polymorphism differed between high‐ and low‐predation populations. Together, this shows that the variation underlying preference could be explained by simple changes in expression and coding of opsins, providing important candidate genes to investigate the genetic basis of female preference variation in this model system.     

Colour‐based foraging diverges after multiple generations under different light environments

When the environment changes, sensory systems can adapt plastically or evolve genetically to the new surroundings, and traits and behaviours reliant on these sensory systems may also change, leading to altered evolutionary trajectories. We tested for differences in colour‐based foraging preferences of guppies (Poecilia reticulata) that lived for 6–10 generations under each of three light environments (green, lilac or control) to determine whether evolution under different light environments alters visually based behaviour. When tested in a common light environment, we found differences in pecking behaviour between treatments that were likely due to changes in the visual system. Pecking behaviour towards green stimuli was consistent across light treatments, possibly reflecting the importance of detecting green algae in the wild. The blue stimulus was only pecked at by fish from the control environments. Behaviour towards long wavelength stimuli varied, possibly due to the polymorphic nature of the long wavelength opsins. These results are consistent with one component of sensory drive but do not allow us to conclude whether these differences are due to plastic or evolved responses.     

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.     

Diel Cycles in Chemosensory Behaviors of Free‐Ranging Rattlesnakes Lying in Wait for Prey

The sensory ecology of foragers is fundamentally influenced by changes in environmental conditions such as ambient light. Changes in ambient light may hinder the effectiveness of particular senses (e.g., impaired vision at night), but many predators rely on multiple sensory systems and may continue to forage despite changes in light availability. Exactly how predator behaviors and sensory systems compensate under changes in light availability in the field is not well understood. We used radio telemetry and portable video surveillance cameras to quantify the sit‐and‐wait chemosensory foraging behavior of free‐ranging red diamond (Crotalus ruber) and northern Pacific (Crotalus oreganus oreganus) rattlesnakes during day and night periods. The two most common behaviors we observed were chemosensory probes, a behavior we describe in detail for the first time, and mouth gapes. During chemosensory probes, rattlesnakes extend their head beyond their coil, explore the surrounding area while tongue‐flicking, and subsequently return to a stationary position inside their coil. Foraging rattlesnakes probed at significantly higher rates during nocturnal vs. diurnal hours. Similarly, mouth gaping occurred during a higher percentage of nocturnal vs. diurnal hours for foraging snakes. Nearly half of all mouth gapes were followed immediately with a chemosensory probe, suggesting that mouth gaping also serves a chemosensory function in this context. Our results suggest that chemical cues play an increasingly important role in mediating rattlesnake foraging behavior at night. Examining how abiotic factors, such as light availability, influence the sensory ecology of free‐ranging predators is essential for accurately characterizing their interactions with prey.     

The insensitivity of thermal preferences to various thermal gradient profiles in newts

Many ectotherms possess the ability to behaviourally regulate their body temperatures. Thermoregulatory behaviour is affected by various biotic and abiotic factors, which may cause a substantial bias in the laboratory estimates of preferred body temperatures (T _p). We examined thermoregulatory behaviour in alpine newts, Ichthyosaura (formerly Triturus) alpestris, in both horizontal linear and vertical nonlinear thermal gradients, to evaluate the influence of a disparate water temperature distribution on their thermal preferences. Newt positions in thermal gradients differed from those in constant temperatures, which indicates their thermal preferences in both experimental setups. The mean and range of body temperatures showed similar values in both types of aquatic thermal gradients. We concluded that under a sufficiently wide range of environmental temperatures, newt thermal preferences are largely insensitive to the thermal gradient profile. This supports the suitability of T _p estimates for further experimental and comparative studies in newts.     

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.     

A genetically explicit model of speciation by sensory drive within a continuous population in aquatic environments

Background  

The sensory drive hypothesis predicts that divergent sensory adaptation in different habitats may lead to premating isolation upon secondary contact of populations. Speciation by sensory drive has traditionally been treated as a special case of speciation as a byproduct of adaptation to divergent environments in geographically isolated populations. However, if habitats are heterogeneous, local adaptation in the sensory systems may cause the emergence of reproductively isolated species from a single unstructured population. In polychromatic fishes, visual sensitivity might become adapted to local ambient light regimes and the sensitivity might influence female preferences for male nuptial color. In this paper, we investigate the possibility of speciation by sensory drive as a byproduct of divergent visual adaptation within a single initially unstructured population. We use models based on explicit genetic mechanisms for color vision and nuptial coloration.     

Change in male coloration associated with artificial selection on foraging colour preference

Sensory drive proposes that natural selection on nonmating behaviours (e.g. foraging preferences) alters sensory system properties and results in a correlated effect on mating preferences and subsequently sexual traits. In colour‐based systems, we can test this by selecting on nonmating colour preferences and testing for responses in colour‐based female preferences and male sexual coloration. In guppies (Poecilia reticulata), individual functional links of sensory drive have been demonstrated providing an opportunity to test the process over more than one link. We measured male coloration and female preferences in populations previously artificially selected for colour‐based foraging behaviour towards two colours, red and blue. We found associated changes in male coloration in the expected direction as well as weak changes in female preferences. Our results can be explained by a correlated response in female preferences due to artificial selection on foraging preferences that are mediated by a shared sensory system or by other mechanisms such as colour avoidance, pleiotropy or social experiences. This is the first experimental evidence that selection on a nonmating behaviour can affect male coloration and, more weakly, female preferences.     

Ontogenetic changes in responses to settlement cues by Anemonefish

Population connectivity for most marine species is dictated by dispersal during the pelagic larval stage. Although reef fish larvae are known to display behavioral adaptations that influence settlement site selection, little is known about the development of behavioral preferences throughout the larval phase. Whether larvae are attracted to the same sensory cues throughout their larval phase, or exhibit distinct ontogenetic shifts in sensory preference is unknown. Here, we demonstrate an ontogenetic shift in olfactory cue preferences for two species of anemonefish, a process that could aid in understanding both patterns of dispersal and settlement. Aquarium-bred na?ve Amphiprion percula and A. melanopus larvae were tested for olfactory preference of relevant reef-associated chemical cues throughout the 11-day pelagic larval stage. Age posthatching had a significant effect on the preference for olfactory cues from host anemones and live corals for both species. Preferences of olfactory cues from tropical plants of A. percula, increased by approximately ninefold between hatching and settlement, with A. percula larvae showing a fivefold increase in preference for the olfactory cue produced by the grass species. Larval age had no effect on the olfactory preference for untreated seawater over the swamp-based tree Melaleuca nervosa, which was always avoided compared with blank seawater. These results indicate that reef fish larvae are capable of utilizing olfactory cues early in the larval stage and may be predisposed to disperse away from reefs, with innate olfactory preferences drawing newly hatched larvae into the pelagic environment. Toward the end of the larval phase, larvae become attracted to the olfactory cues of appropriate habitats, which may assist them in identification of and navigation toward suitable settlement sites.     

Individual differences in temperature perception: Evidence of common processing of sensation intensity of warmth and cold

The longstanding question of whether temperature is sensed via separate sensory systems for warmth and cold was investigated by measuring individual differences in perception of nonpainful heating and cooling. Sixty-two subjects gave separate ratings of the intensity of thermal sensations (warmth, cold) and nociceptive sensations (burning/stinging/pricking) produced by cooling (29°C) or heating (37°C) local regions of the forearm. Stimuli were delivered via a 4?×?4 array of 8 mm?×?8?mm Peltier thermoelectric modules that enabled test temperatures to be presented sequentially to individual modules or simultaneously to the full array. Stimulation of the full array showed that perception of warmth and cold were highly correlated (Pearson r?=?0.83, p?<?0.05). Ratings of nonpainful nociceptive sensations produced by the two temperatures were also correlated, but to a lesser degree (r?=?0.44), and the associations between nociceptive and thermal sensations (r?=?0.35 and 0.22 for 37 and 29°C, respectively) were not significant after correction for multiple statistical tests. Intensity ratings for individual modules indicated that the number of responsive sites out of 16 was a poor predictor of temperature sensations but a significant predictor of nociceptive sensations. The very high correlation between ratings of thermal sensations conflicts with the classical view that warmth and cold are mediated by separate thermal modalities and implies that warm-sensitive and cold-sensitive spinothalamic pathways converge and undergo joint modulation in the central nervous system. Integration of thermal stimulation from the skin and body core within the thermoregulatory system is suggested as the possible source of this convergence.     

Mutation‐order divergence by sexual selection: diversification of sexual signals in similar environments as a first step in speciation

The origin of species remains a central question, and recent research focuses on the role of ecological differences in promoting speciation. Ecological differences create opportunities for divergent selection (i.e. ‘ecological’ speciation), a Darwinian hypothesis that hardly requires justification. In contrast, ‘mutation‐order’ speciation proposes that, instead of adapting to different environments, populations find different ways to adapt to similar environments, implying that speciation does not require ecological differences. This distinction is critical as it provides an alternative hypothesis to the prevailing view that ecological differences drive speciation. Speciation by sexual selection lies at the centre of debates about the importance of ecological differences in promoting speciation; here, we present verbal and mathematical models of mutation‐order divergence by sexual selection. We develop three general cases and provide a two‐locus population genetic model for each. Results indicate that alternative secondary sexual traits can fix in populations that initially experience similar natural and sexual selection and that divergent traits and preferences can remain stable in the face of low gene flow. This stable divergence can facilitate subsequent divergence that completes or reinforces speciation. We argue that a mutation‐order process could explain widespread diversity in secondary sexual traits among closely related, allopatric species.     

Innate preference in Drosophila melanogaster

Innate preference behaviors are fundamental for animal survival. They actually form the basis for many animal complex behaviors. Recent years have seen significant progresses in disclosing the molecular and neural mechanism underlying animal innate preferences, especially in Drosophila. In this review, I will review these studies according to the sensory modalities adopted for preference assaying, such as vision, olfaction, thermal sensation. The behavioral strategies and the theoretic models for the formation of innate preferences are also reviewed and discussed.     

Body temperature and territory selection by males of the speckled wood butterfly (Pararge aegeria): what makes a forest sunlit patch a rendezvous site?

1. Insects locate mobile resources like prey items or mates using either sit‐and‐wait (‘perching’) or active (‘patrolling’) searching strategies. The sit‐and‐wait strategy can be accompanied by defending and monopolising a site through territorial behaviour. 2. The present study focuses on the territorial perching behaviour in males of the speckled wood butterfly (Pararge aegeria L.). Recent studies suggested that the selection of territories (i.e. sunlit patches on the forest floor) is driven by structural characteristics of the site that affect male visual detection. However, given that adult butterflies are heliothermic organisms and that forests provide a diverse array of light environments, it seems likely that thermal aspects may also be used for territory selection. 3. We tested whether used and unused sunlit patches differed in thermal profile under field conditions in a Belgian woodland. We also used dummy butterflies to quantify variation in operative thoracic temperature and to calculate heating rates within (i.e. different vegetation structures) and between patches. 4. Sunlit patches occupied by a territorial male were larger, and were more frequently characterised by low vegetation structures compared with empty sunlit patches. It took longer to reach optimal thorax temperature (starting from a fixed suboptimal body temperature) in small patches compared with large patches. 5. We suggest that aspects of visual detection need to be combined with thermal aspects to fully understand territory selection in the speckled wood butterfly, as synergetic and/or trade‐off effects of ambient temperature, solar radiation, and canopy/vegetation structure may be involved.     

An efficient and inexpensive method for measuring long-term thermoregulatory behavior

Thermoregulatory ability and behavior influence organismal responses to their environment. By measuring thermal preferences, researchers can better understand the effects that temperature tolerances have on ecological and physiological responses to both biotic and abiotic stressors. However, because of funding limitations and confounders, measuring thermoregulation can often be difficult. Here, we provide an effective, affordable (~$50 USD per unit), easy to construct, and validated apparatus for measuring the long-term thermal preferences of animals. In tests, the apparatus spanned temperatures from 9.29 to 33.94 °C, and we provide methods to further increase this range. Additionally, we provide simple methods to non-invasively measure animal and substrate temperatures and to prevent temperature preferences of the focal organisms from being confounded with temperature preferences of its prey and its humidity preferences. To validate the apparatus, we show that it was capable of detecting individual-level consistency and among individual-level variation in the preferred body temperatures of Southern toads (Anaxyrus terrestris) and Cuban tree frogs (Osteopilus septentrionalis) over three-weeks. Nearly every aspect of our design is adaptable to meet the needs of a multitude of study systems, including various terrestrial amphibious, and aquatic organisms. The apparatus and methods described here can be used to quantify behavioral thermal preferences, which can be critical for determining temperature tolerances across species and thus the resiliency of species to current and impending climate change.     

‘Do you remember the first time?’ Host plant preference in a moth is modulated by experiences during larval feeding and adult mating

In insects, like in other animals, experience‐based modulation of preference, a form of phenotypic plasticity, is common in heterogeneous environments. However, the role of multiple fitness‐relevant experiences on insect preference remains largely unexplored. For the multivoltine polyphagous moth Spodoptera littoralis we investigated effects of larval and adult experiences on subsequent reproductive behaviours. We demonstrate, for the first time in male and female insects, that mating experience on a plant modulates plant preference in subsequent reproductive behaviours, whereas exposure to the plant alone or plant together with sex pheromone does not affect this preference. When including larval feeding experiences, we found that both larval rearing and adult mating experiences modulate host plant preference. These findings represent the first evidence that host plant preferences in polyphagous insects are determined by a combination of innate preferences modulated by sensory feedback triggered by multiple rewarding experiences throughout their lifetime.     

Parallel trait adaptation across opposing thermal environments in experimental Drosophila melanogaster populations

Thermal stress is a pervasive selective agent in natural populations that impacts organismal growth, survival, and reproduction. Drosophila melanogaster exhibits a variety of putatively adaptive phenotypic responses to thermal stress in natural and experimental settings; however, accompanying assessments of fitness are typically lacking. Here, we quantify changes in fitness and known thermal tolerance traits in replicated experimental D. melanogaster populations following more than 40 generations of evolution to either cyclic cold or hot temperatures. By evaluating fitness for both evolved populations alongside a reconstituted starting population, we show that the evolved populations were the best adapted within their respective thermal environments. More strikingly, the evolved populations exhibited increased fitness in both environments and improved resistance to both acute heat and cold stress. This unexpected parallel response appeared to be an adaptation to the rapid temperature changes that drove the cycling thermal regimes, as parallel fitness changes were not observed when tested in a constant thermal environment. Our results add to a small, but growing group of studies that demonstrate the importance of fluctuating temperature changes for thermal adaptation and highlight the need for additional work in this area.     

Thermal biology of a colour‐dimorphic snake,Elaphe quadrivirgata,in a montane forest: do melanistic snakes enjoy thermal advantages?

The adaptive significance of colour polymorphisms in animals has received extensive scientific attention. In snakes, a generally accepted hypothesis is that melanistic individuals enjoy thermal advantages compared to normal coloured individuals. Elaphe quadrivirgata on Yakushima Island exhibits a distinct melanistic/striped colour dimorphism. To test this hypothesis, the thermal biology of free‐ranging E. quadrivirgata was investigated using temperature‐sensitive radio transmitters. The thermal quality of habitats was also evaluated using physical models of the snake. In addition, the species' set‐point range (T_set) was estimated using a laboratory experiment. In July, thermal environments appear to be benign because snakes were able to maintain their body temperature (T_b) within T_set from the midday to evening by using average thermal habitats. By contrast, later months of the year were severe in thermoregulation, and snakes had difficulty maintaining their T_b within T_set by using average thermal habitats. There were no significant intermorph differences in thermoregulation indices in any months, whereas slight differences were detected in hourly comparisons. Most of these comparisons indicated active and precise thermoregulation (with respect to T_set) in striped individuals by using thermally favourable but rare microhabitats such as forest gap. Thus, the obtained values do not support the prediction that melanistic individuals are precise thermoregulators. Yet, melanistic individuals do modify their thermoregulation strategy with respect to the available thermal environments in contrast to striped individuals. Together with the fact that body heating is slower in striped individuals than in melanistic individuals under experimental conditions, it is concluded that melanistic individuals have the potential to enjoy thermal advantages but that this might be of no practical use in terms of T_b in the wild because of the greater thermoregulatory efforts of striped individuals, and because melanistic individuals may use forest gap rarely due to conspicuousness to visually orientated predators under the exposed habitat. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 92 , 309–322.     

Genomic characterization of three novel Desulfobacterota classes expand the metabolic and phylogenetic diversity of the phylum

We report on the genomic characterization of three novel classes in the phylum Desulfobacterota. One class (proposed name Candidatus ‘Anaeroferrophillalia’) was characterized by heterotrophic growth capacity, either fermentatively or utilizing polysulfide, tetrathionate or thiosulfate as electron acceptors. In the absence of organic carbon sources, autotrophic growth via the Wood–Ljungdahl (WL) pathway and using hydrogen or Fe(II) as an electron donor is also inferred for members of the ‘Anaeroferrophillalia’. The second class (proposed name Candidatus ‘Anaeropigmentia’) was characterized by its capacity for growth at low oxygen concentration, and the capacity to synthesize the methyl/alkyl carrier CoM, an ability that is prevalent in the archaeal but rare in the bacterial domain. Pigmentation is inferred from the capacity for carotenoid (lycopene) production. The third class (proposed name Candidatus ‘Zymogenia’) was characterized by fermentative heterotrophic growth capacity, broad substrate range and the adaptation of some of its members to hypersaline habitats. Analysis of the distribution pattern of all three classes showed their occurrence as rare community members in multiple habitats, with preferences for anaerobic terrestrial, freshwater and marine environments over oxygenated (e.g. pelagic ocean and agricultural land) settings. Special preference for some members of the class Candidatus ‘Zymogenia’ for hypersaline environments such as hypersaline microbial mats and lagoons was observed.     

Exploring the hidden landscape of female preferences for complex signals

A major challenge in evolutionary biology is explaining the origins of complex phenotypic diversity. In animal communication, complex signals may evolve from simpler signals because novel signal elements exploit preexisting biases in receivers’ sensory systems. Investigating the shape of female preference functions for novel signal characteristics is a powerful, but underutilized, method to describe the adaptive landscape potentially guiding complex signal evolution. We measured female preference functions for characteristics of acoustic appendages added to male calling songs in the grasshopper Chorthippus biguttulus, which naturally produces only simple songs. We discovered both hidden preferences for and biases against novel complex songs, and identified rules governing song attractiveness based on multiple characteristics of both the base song and appendage. The appendage's temporal position and duration were especially important: long appendages preceding the song often made songs less attractive, while following appendages were neutral or weakly attractive. Appendages had stronger effects on songs of shorter duration, but did not restore the attractiveness of very unattractive songs. We conclude that sensory biases favor, within predictable limits, the evolution of complex songs in grasshoppers. The function‐valued approach is an important tool in determining the generality of these limits in other taxa and signaling modalities.