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.     

Depth‐dependent plasticity in opsin gene expression varies between damselfish (Pomacentridae) species

Phenotypic plasticity plays an important role in adapting the visual capability of many animal species to changing sensory requirements. Such variability may be driven by developmental change or may result from environmental changes in light habitat, thereby improving performance in different photic environments. In this study, we examined inter‐ and intraspecific plasticity of visual sensitivities in seven damselfish species, part of the species‐rich and colourful fish fauna of the Great Barrier Reef in Australia. Our goal was to test whether the visual systems of damselfish were tuned to the prevailing light environment in different habitats and/or other aspects of their lifestyle. More specifically, we compared the opsin gene expression levels from individuals living in different photic habitats. We found that all species expressed rod opsin (RH1) used for dim‐light vision, and primarily three cone opsins (SWS1, RH2B and RH2A) used for colour vision. While RH1 levels changed exclusively following a diurnal cycle, cone opsin expression varied with depth in four of the seven species. Estimates of visual pigment performance imply that changes in opsin expression adjust visual sensitivities to the dominant photic regime. However, we also discovered that some species show a more stable opsin expression profile. Further, we found indication that seasonal changes, possibly linked to changes in the photic environment, might also trigger opsin expression. These findings suggest that plasticity in opsin gene expression of damselfish is highly species‐specific, possibly due to ecological differences in visual tasks or, alternatively, under phylogenetic constraints.     

Plasticity of opsin gene expression in cichlids from Lake Malawi

Sensory systems play crucial roles in survival and reproduction. Therefore, sensory plasticity has important evolutionary implications. In this study, we examined retinal plasticity in five species of cichlid fish from Lake Malawi. We compared the cone opsin expression profiles of wild‐caught fish to lab‐reared F₁ that had been raised in a UV minus, reduced intensity light environment. All of the opsin genes that were expressed in wild‐caught fish were also expressed in lab‐reared individuals. However, we found statistically significant differences in relative opsin expression among all five species. The most consistent difference was in the SWS2B (violet) opsin, which was always expressed at higher levels in lab‐reared individuals. Estimates of visual pigment quantum catch suggest that this change in expression would increase retinal sensitivity in the light environment of the lab. We also found that the magnitude of plasticity varied across species. These findings have important implications for understanding the genetic regulation of opsin expression and raise many interesting questions about how the cichlid visual system develops. They also suggest that sensory plasticity may have facilitated the ecological diversification of cichlids in Lake Malawi.     

Insect mating signal and mate preference phenotypes covary among host plant genotypes

Sexual selection acting on small initial differences in mating signals and mate preferences can enhance signal–preference codivergence and reproductive isolation during speciation. However, the origin of initial differences in sexual traits remains unclear. We asked whether biotic environments, a source of variation in sexual traits, may provide a general solution to this problem. Specifically, we asked whether genetic variation in biotic environments provided by host plants can result in signal–preference phenotypic covariance in a host‐specific, plant‐feeding insect. We used a member of the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae) to assess patterns of variation in male mating signals and female mate preferences induced by genetic variation in host plants. We employed a novel implementation of a quantitative genetics method, rearing field‐collected treehoppers on a sample of naturally occurring replicated host plant clone lines. We found remarkably high signal–preference covariance among host plant genotypes. Thus, genetic variation in biotic environments influences the sexual phenotypes of organisms living on those environments in a way that promotes assortative mating among environments. This consequence arises from conditions likely to be common in nature (phenotypic plasticity and variation in biotic environments). It therefore offers a general answer to how divergent sexual selection may begin.     

Diurnal lighting patterns and habitat alter opsin expression and colour preferences in a killifish

Spatial variation in lighting environments frequently leads to population variation in colour patterns, colour preferences and visual systems. Yet lighting conditions also vary diurnally, and many aspects of visual systems and behaviour vary over this time scale. Here, we use the bluefin killifish (Lucania goodei) to compare how diurnal variation and habitat variation (clear versus tannin-stained water) affect opsin expression and the preference to peck at different-coloured objects. Opsin expression was generally lowest at midnight and dawn, and highest at midday and dusk, and this diurnal variation was many times greater than variation between habitats. Pecking preference was affected by both diurnal and habitat variation but did not correlate with opsin expression. Rather, pecking preference matched lighting conditions, with higher preferences for blue at noon and for red at dawn/dusk, when these wavelengths are comparatively scarce. Similarly, blue pecking preference was higher in tannin-stained water where blue wavelengths are reduced. In conclusion, L. goodei exhibits strong diurnal cycles of opsin expression, but these are not tightly correlated with light intensity or colour. Temporally variable pecking preferences probably result from lighting environment rather than from opsin production. These results may have implications for the colour pattern diversity observed in these fish.     

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.     

Sexual selection on Drosophila serrata male pheromones does not vary with female age or mating status

Mate preferences are costly and are thought to evolve due to the direct and/or indirect benefits they provide. Such costs and benefits may vary in response to intrinsic and extrinsic factors with important evolutionary consequences. Limited attention has been given to quantifying such variation and understanding its causes, most notably with respect to the direction and strength of preferences for multivariate sexual displays. In Drosophila serrata, female preferences target a pheromone blend of long‐chain cuticular hydrocarbons (CHCs). We used a factorial design to test whether female age and mating status generated variation in the strength and direction of sexual selection on male CHCs. Replicate choice mating trials were conducted using young and old females (4 or 10 days post‐emergence) that were either virgin or previously mated. The outcome of such trials is known to capture variation in female mate preferences, although male–male interactions may also contribute. Directional sexual selection on male CHCs was highly significant within each treatment, but there was little evidence of any variation among treatments. The absence of treatment effects implies that the multivariate combination of male CHCs preferred by females was constant with respect to female age and mating status. To the extent that male–male interactions may also contribute, our results similarly imply that these did not vary among treatments groups. With respect to D. serrata mate preferences, our results suggest that either plasticity with respect to age and mating status is not beneficial to females, or preference expression is somehow constrained.     

Adult plasticity in African cichlids: Rapid changes in opsin expression in response to environmental light differences

Phenotypic plasticity allows organisms to adapt quickly to local environmental conditions and could facilitate adaptive radiations. Cichlids have recently undergone an adaptive radiation in Lake Malawi where they inhabit diverse light environments and tune their visual sensitivity through differences in cone opsin expression. While cichlid opsin expression is known to be plastic over development, whether adults remain plastic is unknown. Adult plasticity in visual tuning could play a role in cichlid radiations by enabling survival in changing environments and facilitating invasion into novel environments. Here we examine the existence of and temporal changes in adult visual plasticity of two closely related species. In complementary experiments, wild adult Metriaclima mbenji from Lake Malawi were moved to the lab under UV‐deficient fluorescent lighting; while lab raised M. benetos were placed under UV‐rich lighting designed to mimic light conditions in the wild. Surprisingly, adult cichlids in both experiments showed significant changes in the expression of the UV‐sensitive single cone opsin, SWS1, in only 3 days. Modeling quantum catches in the light environments revealed a possible link between the light available to the SWS1 visual pigment and SWS1 expression. We conclude that adult cichlids can undergo rapid and significant changes in opsin expression in response to environmental light shifts that are relevant to their habitat and evolutionary history in Lake Malawi. This could have contributed to the rapid divergence characteristic of these fantastic fishes.     

Relative LWS cone opsin expression determines optomotor thresholds in Malawi cichlid fish

Associating quantitative genetic traits with quantitative behaviors is a relatively unexplored region of sensory neurobiology. The visual system is an ideal place to test models associating these levels of sensory perception. In this study, we reared cichlid fish from Lake Malawi in different ambient light environments. We then tested the visual sensitivities of these fish using the optomotor response (OMR) behavioral paradigm and measured the relative expression of cone opsin genes. We found that the light environment experienced by fish during development can alter gene expression, particularly as it applies to the long wavelength-sensitive (LWS) opsin gene. Also, fish from different rearing conditions exhibited different behavioral sensitivities. We combined these data with predictions of opsin pigment absorption by the different OMR stimuli to determine which cone types are most likely to influence the OMR behavior. While we hypothesized that this behavior would be controlled by a random-wiring model reflecting the expression of both medium wavelength-sensitive (MWS) and LWS opsins, our models suggest that only the LWS pigment is required to predict behavior. Furthermore, analyses show that LWS expression variation accounts for ~20% of the observed behavioral variance. This work confirms that sensory gene expression influences behavior in a predictable fashion. It also suggests that the neural wiring of basal visual pathways in cichlid fish may differ from that observed in mammals and zebrafish, but is similar to that described in goldfish. This finding has important implications for the evolution of the magnocellular neural pathway in teleosts.     

Why do ovigerous females approach courting males? Female preferences and sensory biases in a fiddler crab

Perceptual biases explain the origin and evolution of female preference in many species. Some responses that mediate mate choice, however, may have never been used in nonmating contexts. In the fiddler crab, Uca mjoebergi, mate‐searching females prefer faster wave rates and leading wave; however, it remains unclear whether such responses evolved in a mating context (i.e., the preference has effect on the fitness of the female and her offspring that arise from mating with a particular male) or a nonmating contexts (i.e., a female obtains direct benefits through selecting the male with a more detectable trait). Here, we compared the preferences of mate‐searching with those of ovigerous females that are searching for a burrow and do not concern about male “quality.” Results showed that as both mate‐searching and ovigerous females preferentially approached robotic males with faster wave rates. This suggests that wave rate increases detectability/locatability of males, but the mating preference for this trait is unlikely to evolve in the mating context (although it may currently function in mate choice), as it does not provide fitness‐related benefit to females or her offspring. Wave leadership, in contract, was attractive to mate‐searching females, but not ovigerous females, suggesting that female preference for leadership evolves because wave leadership conveys information about male quality. We provide not only an empirical evidence of sensory biases (in terms of the preference for faster wave), but the first experimental evidence that mating context can be the only selection force that mediates the evolution of male sexual traits and female preference (in terms of the preference for leading wave).     

Temperature coupling of mate attraction signals and female mate preferences in four populations of Enchenopa treehopper (Hemiptera: Membracidae)

Variation in temperature can affect the expression of a variety of important fitness‐related behaviours, including those involved with mate attraction and selection, with consequences for the coordination of mating across variable environments. We examined how temperature influences the expression of male mating signals and female mate preferences—as well as the relationship between how male signals and female mate preferences change across temperatures (signal–preference temperature coupling)—in Enchenopa binotata treehoppers. These small plant‐feeding insects communicate using plantborne vibrations, and our field surveys indicate they experience significant natural variation in temperature during the mating season. We tested for signal–preference temperature coupling in four populations of E. binotata by manipulating temperature in a controlled laboratory environment. We measured the frequency of male signals—the trait for which females show strongest preference—and female peak preference—the signal frequency most preferred by females—across a range of biologically relevant temperatures (18°C–36°C). We found a strong effect of temperature on both male signals and female preferences, which generated signal–preference temperature coupling within each population. Even in a population in which male signals mismatched female preferences, the temperature coupling reinforces predicted directional selection across all temperatures. Additionally, we found similar thermal sensitivity in signals and preferences across populations even though populations varied in the mean frequency of male signals and female peak preference. Together, these results suggest that temperature variation should not affect the action of sexual selection via female choice, but rather should reinforce stabilizing selection in populations with signal–preference matches, and directional selection in those with signal–preference mismatches. Finally, we do not predict that thermal variation will disrupt the coordination of mating in this species by generating signal–preference mismatches at thermal extremes.     

Female mating preferences and male coloration covary with water transparency in a Lake Victoria cichlid fish

Rapid speciation in Lake Victoria cichlid fish of the genus Pundamilia may be facilitated by sexual selection: female mate choice exerts sexual selection on male nuptial coloration within species and maintains reproductive isolation between species. However, declining water transparency coincides with increasingly dull coloration and increasing hybridization. In the present study, we investigated the mechanism underlying this pattern in Pundamilia nyererei, a species that interbreeds with a sister species in turbid but not in clear water. We compared measures of intraspecific sexual selection between two populations from locations that differ in water transparency. First, in laboratory mate‐choice experiments, conducted in clear water and under broad‐spectrum illumination, we found that females originating from turbid water have significantly weaker preferences for male coloration than females originating from clear water. Second, both the hue and body coverage of male coloration differ between populations, which is consistent with adaptation to different photic habitats. These findings suggest that the observed relationship between male coloration and water transparency is not mediated by environmental variation alone. Rather, female mating preferences are indicated to have changed in response to this variation, constituting the first evidence for intraspecific preference‐trait co‐evolution in cichlid fish. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 398–406.     

Independent Mating Preferences for Male Body Size and Coloration in Female Trinidadian Guppies

Although females in numerous species generally prefer males with larger, brighter and more elaborate sexual traits, there is nonetheless considerable intra‐ and interpopulation variation in mating preferences amongst females that requires explanation. Such variation exists in the Trinidadian guppy, Poecilia reticulata, an important model organism for the study of sexual selection and mate choice. While female guppies tend to prefer more ornamented males as mates, particularly those with greater amounts of orange coloration, there remains variation both in male traits and female mating preferences within and between populations. Male body size is another trait that is sexually selected through female mate choice in some species, but has not been examined as extensively as body coloration in the guppy despite known intra‐ and interpopulation variation in this trait among adult males and its importance for survivorship in this species. In this study, we used a dichotomous‐choice test to quantify the mating preferences of female guppies, originating from a low‐predation population in Trinidad, for two male traits, body length and area of the body covered with orange and black pigmentation, independently of each other. We expected strong female mating preferences for both male body length and coloration in this population, given relaxation from predation and presumably relatively low cost of choice. Females indeed exhibited a strong preference for larger males as expected, but surprisingly a weaker (but nonetheless significant) preference for orange and black coloration. Interestingly, larger females demonstrated stronger preferences for larger males than did smaller females, which could potentially lead to size‐assortative mating in nature.     

Rapid adaptation to a novel light environment: The importance of ontogeny and phenotypic plasticity in shaping the visual system of Nicaraguan Midas cichlid fish (Amphilophus citrinellus spp.)

Colonization of novel habitats is typically challenging to organisms. In the initial stage after colonization, approximation to fitness optima in the new environment can occur by selection acting on standing genetic variation, modification of developmental patterns or phenotypic plasticity. Midas cichlids have recently colonized crater Lake Apoyo from great Lake Nicaragua. The photic environment of crater Lake Apoyo is shifted towards shorter wavelengths compared to great Lake Nicaragua and Midas cichlids from both lakes differ in visual sensitivity. We investigated the contribution of ontogeny and phenotypic plasticity in shaping the visual system of Midas cichlids after colonizing this novel photic environment. To this end, we measured cone opsin expression both during development and after experimental exposure to different light treatments. Midas cichlids from both lakes undergo ontogenetic changes in cone opsin expression, but visual sensitivity is consistently shifted towards shorter wavelengths in crater lake fish, which leads to a paedomorphic retention of their visual phenotype. This shift might be mediated by lower levels of thyroid hormone in crater lake Midas cichlids (measured indirectly as dio2 and dio3 gene expression). Exposing fish to different light treatments revealed that cone opsin expression is phenotypically plastic in both species during early development, with short and long wavelength light slowing or accelerating ontogenetic changes, respectively. Notably, this plastic response was maintained into adulthood only in the derived crater lake Midas cichlids. We conclude that the rapid evolution of Midas cichlids’ visual system after colonizing crater Lake Apoyo was mediated by a shift in visual sensitivity during ontogeny and was further aided by phenotypic plasticity during development.     

Mechanisms of species divergence through visual adaptation and sexual selection: Perspectives from a cichlid model sys-tem

The theory of ecological speciation suggests that assortative mating evolves most easily when mating preferences are directly linked to ecological traits that are subject to divergent selection. Sensory adaptation can play a major role in this process, because selective mating is often mediated by sexual signals: bright colours, complex song, pheromone blends and so on. When divergent sensory adaptation affects the perception of such signals, mating patterns may change as an immediate consequence. Alternatively, mating preferences can diverge as a result of indirect effects: assortative mating may be promoted by selection against intermediate phenotypes that are maladapted to their (sensory) environment. For Lake Victoria cichlids, the visual envi-ronment constitutes an important selective force that is heterogeneous across geographical and water depth gradients. We investi-gate the direct and indirect effects of this heterogeneity on the evolution of female preferences for alternative male nuptial colours (red and blue) in the genus Pundamilia. Here, we review the current evidence for divergent sensory drive in this system, extract general principles, and discuss future perspectives.     

Evolution of opsin expression in birds driven by sexual selection and habitat

Theories of sexual and natural selection predict coevolution of visual perception with conspecific colour and/or the light environment animals occupy. One way to test these theories is to focus on the visual system, which can be achieved by studying the opsin-based visual pigments that mediate vision. Birds vary greatly in colour, but opsin gene coding sequences and associated visual pigment spectral sensitivities are known to be rather invariant across birds. Here, I studied expression of the four cone opsin genes (Lws, Rh2, Sws2 and Sws1) in 16 species of New World warblers (Parulidae). I found levels of opsin expression vary both across species and between the sexes. Across species, female, but not male Sws2 expression is associated with an index of sexual selection, plumage dichromatism. This fits predictions of classic sexual selection models, in which the sensory system changes in females, presumably impacting female preference, and co-evolves with male plumage. Expression of the opsins at the extremes of the light spectrum, Lws and Uvs, correlates with the inferred light environment occupied by the different species. Unlike opsin spectral tuning, regulation of opsin gene expression allows for fast adaptive evolution of the visual system in response to natural and sexual selection, and in particular, sex-specific selection pressures.     

Plasticity of the mate choice mind: courtship evokes choice‐like brain responses in females from a coercive mating system

Female mate choice is fundamental to sexual selection, and determining molecular underpinnings of female preference variation is important for understanding mating character evolution. Previously it was shown that whole‐brain expression of a synaptic plasticity marker, neuroserpin, positively correlates with mating bias in the female choice poeciliid, Xiphophorus nigrensis, when exposed to conspecific courting males, whereas this relationship is reversed in Gambusia affinis, a mate coercive poeciliid with no courting males. Here we explore whether species‐level differences in female behavioral and brain molecular responses represent ‘canalized’ or ‘plastic’ traits. We expose female G. affinis to conspecific males and females, as well as coercive and courting male Poecilia latipinna, for preference assays followed by whole‐brain gene expression analyses of neuroserpin, egr‐1 and early B. We find positive correlations between gene expression and female preference strength during exposure to courting heterospecific males, but a reversed pattern following exposure to coercive heterospecific males. This suggests that the neuromolecular processes associated with female preference behavior are plastic and responsive to different male phenotypes (courting or coercive) rather than a canalized response linked to mating system. Further, we propose that female behavioral plasticity may involve learning because female association patterns shifted with experience. Compared to younger females, we found larger, more experienced females spend less time near coercive males but associate more with males in the presence of courters. We thus suggest a conserved learning‐based neuromolecular process underlying the diversity of female mate preference across the mate choice and coercion‐driven mating systems.     

Covariation and repeatability of male mating effort and mating preferences in a promiscuous fish

Although mate choice by males does occur in nature, our understanding of its importance in driving evolutionary change remains limited compared with that for female mate choice. Recent theoretical models have shown that the evolution of male mate choice is more likely when individual variation in male mating effort and mating preferences exist and positively covary within populations. However, relatively little is known about the nature of such variation and its maintenance within natural populations. Here, using the Trinidadian guppy (Poecilia reticulata) as a model study system, we report that mating effort and mating preferences in males, based on female body length (a strong correlate of fecundity), positively covary and are significantly variable among subjects. Individual males are thus consistent, but not unanimous, in their mate choice. Both individual mating effort (including courtship effort) and mating preference were significantly repeatable. These novel findings support the assumptions and predictions of recent evolutionary models of male mate choice, and are consistent with the presence of additive genetic variation for male mate choice based on female size in our study population and thus with the opportunity for selection and further evolution of large female body size through male mate choice.     

Evolutionary ecology of opsin gene sequence,expression and repertoire

Linking molecular evolution to biological function is a long‐standing challenge in evolutionary biology. Some of the best examples of this involve opsins, the genes that encode the molecular basis of light reception. In this issue of Molecular Ecology, three studies examine opsin gene sequence, expression and repertoire to determine how natural selection has shaped the visual system. First, Escobar‐Camacho et al. ( 2017 ) use opsin repertoire and expression in three Amazonian cichlid species to show that a shift in sensitivity towards longer wavelengths is coincident with the long‐wavelength‐dominated Amazon basin. Second, Stieb et al. ( 2017 ) explore opsin sequence and expression in reef‐dwelling damselfish and find that UV‐ and long‐wavelength vision are both important, but likely for different ecological functions. Lastly, Suvorov et al. ( 2017 ) study an expansive opsin repertoire in the insect order Odonata and find evidence that copy number expansion is consistent with the permanent heterozygote model of gene duplication. Together these studies emphasize the utility of opsin genes for studying both the local adaptation of sensory systems and, more generally, gene family evolution.