Adaptive evolution of butterfly wing shape: from morphology to behaviour

International audienceButterflies display extreme variation in wing shape associated with tremendous ecological diversity. Disentangling the role of neutral versus adaptive processes in wing shape diversification remains a challenge for evolutionary biologists. Ascertaining how natural selection influences wing shape evolution requires both functional studies linking morphology to flight performance, and ecological investigations linking performance in the wild with fitness. However, direct links between morphological variation and fitness have rarely been established. The functional morphology of butterfly flight has been investigated but selective forces acting on flight behaviour and associated wing shape have received less attention. Here, we attempt to estimate the ecological relevance of morpho-functional links established through biomechanical studies in order to understand the evolution of butterfly wing morphology. We survey the evidence for natural and sexual selection driving wing shape evolution in butterflies, and discuss how our functional knowledge may allow identification of the selective forces involved, at both the macro-and micro-evolutionary scales. Our review shows that although correlations between wing shape variation and ecological factors have been established at the macro-evolutionary level, the underlying selective pressures often remain unclear. We identify the need to investigate flight behaviour in relevant ecological contexts to detect variation in fitness-related traits. Identifying the selective regime then should guide experimental studies towards the relevant estimates of flight performance. Habitat, predators and sex-specific behaviours are likely to be major selective forces acting on wing shape evolution in butterflies. Some striking cases of morphological divergence driven by contrasting ecology involve both wing and body morphology, indicating that their interactions should be included in future studies investigating co-evolution between morphology and flight behaviour

The Evolution of Anti-Bat Sensory Illusions in Moths

Prey transmit sensory illusions to redirect predatory strikes, creating a discrepancy between what a predator perceives and reality. We use the acoustic arms race between bats and moths to investigate the evolution and function of a sensory illusion. The spinning hindwing tails of silk moths (Saturniidae) divert bat attack by reflecting sonar to create a misleading echoic target. We characterized geometric morphometrics of moth hindwings across silk moths, mapped these traits onto a new, robust phylogeny, and found that elaborated hindwing structures have converged on four adaptive shape peaks. To test the mechanism underlying these anti-bat traits, we pit bats against three species of silk moths with experimentally altered hindwings that created a representative gradient of ancestral and extant hindwing shapes. High-speed videography of battles reveals that moths with longer hindwings and tails more successfully divert bat attack. We postulate that sensory illusions are widespread and are underappreciated drivers of diversity across systems

Two sisters in the same dress: Heliconius cryptic species

<p>Abstract</p> <p>Background</p> <p>Sister species divergence and reproductive isolation commonly results from ecological adaptation. In mimetic <it>Heliconius </it>butterflies, shifts in colour pattern contribute to pre- and post-mating reproductive isolation and are commonly correlated with speciation. Closely related mimetic species are therefore not expected, as they should lack several important sources of reproductive isolation.</p> <p>Results</p> <p>Here we present phenotypic, behavioral and genetic evidence for the coexistence of two sympatric 'cryptic' species near Florencia in the eastern Andes of Colombia that share the same orange rayed colour pattern. These represent <it>H. melpomene malleti </it>and a novel taxon in the <it>H. cydno </it>group, here designated as novel race of <it>Heliconius timareta</it>, <it>Heliconius timareta florencia</it>. No-choice mating experiments show that these sympatric forms have strong assortative mating (≈96%) despite great similarity in colour pattern, implying enhanced divergence in pheromonal signals.</p> <p>Conclusion</p> <p>We hypothesize that these species might have resulted from recent convergence in colour pattern, perhaps facilitated by hybrid introgression of wing pattern genes.</p

Processing of sky compass cues and wide-field motion in the central complex of the desert locust (Schistocerca gregaria)

1. Polarization-sensitive neurons of the locust central complex show azimuthdependent responses to unpolarized light spots. This suggests that direct sunlight supports the sky polarization compass in this brain area. / 2. In the brain of the desert locust, neurons sensitive to the plane of celestial polarization are arranged like a compass in the slices of the central complex. These neurons, in addition, code for the horizontal direction of an unpolarized light cue possibly representing the sun. We show here that horizontal directions are, in addition to E-vector orientations from dorsal direction, represented in a compass-like manner across the slices of the central complex. However, both compasses are not linked to each other but seem to interact in a cell specific nonlinear way. Our study confirms the role of the central complex in signaling heading directions signaling and shows that different cues are employed for this task. / 3. Visual cues are essential for animal navigation and spatial orientation. Many insects rely on celestial cues for spatial orientation, including the sky polarization pattern. In desert locusts neurons encoding the plane of polarized light (E-vector) are located in the central complex (CX), a group of midline-spanning neuropils. Several types of CX neuron signalling heading direction represent zenithal Evectors in a topographic manner across the slices of the CX and, likely, act as an internal sky compass. Because animals experience optic flow stimulation during flight, we asked whether progressive wide-field motion affects the responses of CX neurons to polarized light. In most neurons, progressive motion disadapted the response to the preferred E-vector (i.e. the E-vector eliciting strongest firing), whereas the response to the anti-preferred E-vector remained comparatively unaffected. This suggests context-dependent gain modulation in sky compass signalling. Three types of compass neuron were responsive to motion simulating body rotation around the yaw axis. Depending on arborization domains in the CX and rotation direction these neurons were strongly excited or inhibited. As proposed for Drosophila, they may be involved in shifting compass signal activity across the slices of the CX as the animal turns enabling it to keep track of its heading

Spectacular pehnomena and limits to rationality in genetic and cultural evolution

In studies of both animal and human behaviour, game theory is used as a tool for understanding strategies that appear in interactions between individuals. Game theory focuses on adaptive behaviour, which can be attained only at evolutionary equilibrium. Here we suggest that behaviour appearing during interactions is often outside the scope of such analysis. In many types of interaction, conflicts of interest exist between players, fueling the evolution of manipulative strategies. Such strategies evolve out of equilibrium, commonly appearing as spectacular morphology or behaviour with obscure meaning, to which other players may react in non-adaptive, irrational way approach, and outline the conditions in which evolutionary equilibria cannot be maintained. Evidence from studies of biological interactions seems to support the view that behaviour is often not at equilibrium. This also appears to be the case for many human cultural traits, which have spread rapidly despite the fact that they have a negative influence on reproduction

Processing of sky compass cues and wide-field motion in the central complex of the desert locust (Schistocerca gregaria)

1. Polarization-sensitive neurons of the locust central complex show azimuthdependent responses to unpolarized light spots. This suggests that direct sunlight supports the sky polarization compass in this brain area. / 2. In the brain of the desert locust, neurons sensitive to the plane of celestial polarization are arranged like a compass in the slices of the central complex. These neurons, in addition, code for the horizontal direction of an unpolarized light cue possibly representing the sun. We show here that horizontal directions are, in addition to E-vector orientations from dorsal direction, represented in a compass-like manner across the slices of the central complex. However, both compasses are not linked to each other but seem to interact in a cell specific nonlinear way. Our study confirms the role of the central complex in signaling heading directions signaling and shows that different cues are employed for this task. / 3. Visual cues are essential for animal navigation and spatial orientation. Many insects rely on celestial cues for spatial orientation, including the sky polarization pattern. In desert locusts neurons encoding the plane of polarized light (E-vector) are located in the central complex (CX), a group of midline-spanning neuropils. Several types of CX neuron signalling heading direction represent zenithal Evectors in a topographic manner across the slices of the CX and, likely, act as an internal sky compass. Because animals experience optic flow stimulation during flight, we asked whether progressive wide-field motion affects the responses of CX neurons to polarized light. In most neurons, progressive motion disadapted the response to the preferred E-vector (i.e. the E-vector eliciting strongest firing), whereas the response to the anti-preferred E-vector remained comparatively unaffected. This suggests context-dependent gain modulation in sky compass signalling. Three types of compass neuron were responsive to motion simulating body rotation around the yaw axis. Depending on arborization domains in the CX and rotation direction these neurons were strongly excited or inhibited. As proposed for Drosophila, they may be involved in shifting compass signal activity across the slices of the CX as the animal turns enabling it to keep track of its heading

Field Studies Reveal Strong Postmating Isolation between Ecologically Divergent Butterfly Populations

A mismatch between hybrid butterflies and their ecological environment restricts gene flow between populations that feed on different host plants, highlighting the potential importance of a seldom-studied mechanism of reproductive isolation

Biogeography of species richness gradients:Linking adaptive traits, demography and diversification

Here we review how adaptive traits contribute to the emergence and maintenance of species richness gradients through their influence on demographic and diversification processes. We start by reviewing how demographic dynamics change along species richness gradients. Empirical studies show that geographical clines in population parameters and measures of demographic variability are frequent along latitudinal and altitudinal gradients. Demographic variability often increases at the extremes of regional species richness gradients and contributes to shape these gradients. Available studies suggest that adaptive traits significantly influence demographic dynamics, and set the limits of species distributions. Traits related to thermal tolerance, resource use, phenology and dispersal seem to play a significant role. For many traits affecting demography and/or diversification processes, complex mechanistic approaches linking genotype, phenotype and fitness are becoming progressively available. In several taxa, species can be distributed along adaptive trait continuums, i.e. a main axis accounting for the bulk of inter-specific variation in some correlated adaptive traits. It is shown that adaptive trait continuums can provide useful mechanistic frameworks to explain demographic dynamics and diversification in species richness gradients. Finally, we review the existence of sequences of adaptive traits in phylogenies, the interactions of adaptive traits and community context, the clinal variation of traits across geographical gradients, and the role of adaptive traits in determining the history of dispersal and diversification of clades. Overall, we show that the study of demographic and evolutionary mechanisms that shape species richness gradients clearly requires the explicit consideration of adaptive traits. To conclude, future research lines and trends in the field are briefly outlined