ROLE OF NATURAL AND SEXUAL SELECTION IN THE EVOLUTION OF BUTTERFLY WING COLOURS

Ph.DDOCTOR OF PHILOSOPH

The functional significance of colour polymorphism in the European common wall lizard (Podarcis muralis)

Colour polymorphisms, the coexistence of two or more colour morphs of a species within a population, have long fascinated evolutionary biologists interested in the mechanisms generating and maintaining phenotypic variation in nature. The functional significance of colour polymorphisms (i.e. their adaptive value) is often linked to the selective mechanisms responsible for their maintenance over time. In lizards, the hypothesis that colour morphs may reflect alternative reproductive strategies involving differential sociosexual behaviour and/or alternative reproductive strategies has come to dominate the field. Wall lizards (family Lacertidae, genus Podarcis), with several geographically distant species that exhibit two or more alternative ventral colour morphs, have often been identified as a group in which alternative reproductive strategies and frequency-dependent selection likely underpin colour polymorphisms. However, several key aspects regarding the link between behaviour, fitness, and lacertid colour polymorphism remain overlooked or inadequately studied. In this thesis we tried to fill these gaps by experimentally addressing some of the most commonly assumed ideas about the functional significance of colour polymorphism in the European common wall lizard (Podarcis muralis, Laurenti 1768). In some populations of this species (e.g. eastern Pyrenees), adult lizards of both sexes may show up to three “pure” alternative colour morph (orange, white, yellow), and two mixed morphs consisting of a mosaic of differently-coloured scales (orange-white, yellow-orange). Although colour morphs are frequently thought to function as social signals mediating intraspecific interactions, morph categorization has been never assessed from the viewpoint of the intended receivers (i.e. conspecifics). Here, using a discrimination experiment and visual modelling, we found that lizards likely perceive the alternative colour morphs as chromatically distinct and show evidence of discriminating among them based on hue, rather than luminance. To evaluate the role of male coloration (including alternative colour morphs) in intra-sexual competition), we conducted lab-staged dyadic contests among size-matched males. We found lower fighting ability in lizards showing a smaller fraction of their outer ventral scales covered with dark melanin-based spots, and in lizards with orange ventral colour (which could result from the existence of a subordinate non-territorial strategy in this morph). However, our results in later studies (with a free-ranging population and ten experimental mesocosm enclosures), strongly refute the hypothesis that alternative socio-sexual behaviour or space use strategies characterize colour morphs when lizards interact under more natural conditions. In the free-ranging populations, colour morphs did not differ in inter-annual site-fidelity, home-range size, or male-female overlap. In the mesocosm enclosures, spatial dominance was the prime determinant of male fitness across colour morphs. In a later experiment, we conducted controlled matings among pure colour morphs and found no overall effect of female morph on clutch size or juvenile mass, and no effect of morph combination on offspring viability or prospective fitness. These results refute the existence of alternative reproductive strategies in female morphs and are also in disagreement with predictions from both correlational selection and heterosis. Lastly, by keeping the juveniles of known crosses in outdoor enclosures for a year, we studied the inheritance and ontogeny of P. muralis colour polymorphism. Specifically, our results confirmed that orange and yellow colour expression depends on two recessive alleles located at two separate autosomal loci and revealed that the whitish coloration exhibited by newborn lizards is likely perceived by conspecifics as a chromatically distinct colour different from any of the morph colours expressed by adult lizards. Overall, in this thesis we have hopefully presented compelling arguments to revise our perspective on the functional significance of lacertid colour polymorphisms, suggested promising lines of research for future work, and generally contributed to our understanding of the processes maintaining intra-specific variation in natural populations at large.Colour polymorphisms, the coexistence of two or more colour morphs of a species within a population, have long fascinated evolutionary biologists interested in the mechanisms generating and maintaining phenotypic variation in nature. The functional significance of colour polymorphisms (i.e. their adaptive value) is often linked to the selective mechanisms responsible for their maintenance over time. In lizards, the hypothesis that colour morphs may reflect alternative reproductive strategies involving differential sociosexual behaviour and/or alternative reproductive strategies has come to dominate the field. Wall lizards (family Lacertidae, genus Podarcis), with several geographically distant species that exhibit two or more alternative ventral colour morphs, have often been identified as a group in which alternative reproductive strategies and frequency-dependent selection likely underpin colour polymorphisms. However, several key aspects regarding the link between behaviour, fitness, and lacertid colour polymorphism remain overlooked or inadequately studied. In this thesis we tried to fill these gaps by experimentally addressing some of the most commonly assumed ideas about the functional significance of colour polymorphism in the European common wall lizard (Podarcis muralis, Laurenti 1768). In some populations of this species (e.g. eastern Pyrenees), adult lizards of both sexes may show up to three “pure” alternative colour morph (orange, white, yellow), and two mixed morphs consisting of a mosaic of differently-coloured scales (orange-white, yellow-orange). Although colour morphs are frequently thought to function as social signals mediating intraspecific interactions, morph categorization has been never assessed from the viewpoint of the intended receivers (i.e. conspecifics). Here, using a discrimination experiment and visual modelling, we found that lizards likely perceive the alternative colour morphs as chromatically distinct and show evidence of discriminating among them based on hue, rather than luminance. To evaluate the role of male coloration (including alternative colour morphs) in intra-sexual competition), we conducted lab-staged dyadic contests among size-matched males. We found lower fighting ability in lizards showing a smaller fraction of their outer ventral scales covered with dark melanin-based spots, and in lizards with orange ventral colour (which could result from the existence of a subordinate non-territorial strategy in this morph). However, our results in later studies (with a free-ranging population and ten experimental mesocosm enclosures), strongly refute the hypothesis that alternative socio-sexual behaviour or space use strategies characterize colour morphs when lizards interact under more natural conditions. In the free-ranging populations, colour morphs did not differ in inter-annual site-fidelity, home-range size, or male-female overlap. In the mesocosm enclosures, spatial dominance was the prime determinant of male fitness across colour morphs. In a later experiment, we conducted controlled matings among pure colour morphs and found no overall effect of female morph on clutch size or juvenile mass, and no effect of morph combination on offspring viability or prospective fitness. These results refute the existence of alternative reproductive strategies in female morphs and are also in disagreement with predictions from both correlational selection and heterosis. Lastly, by keeping the juveniles of known crosses in outdoor enclosures for a year, we studied the inheritance and ontogeny of P. muralis colour polymorphism. Specifically, our results confirmed that orange and yellow colour expression depends on two recessive alleles located at two separate autosomal loci and revealed that the whitish coloration exhibited by newborn lizards is likely perceived by conspecifics as a chromatically distinct colour different from any of the morph colours expressed by adult lizards. Overall, in this thesis we have hopefully presented compelling arguments to revise our perspective on the functional significance of lacertid colour polymorphisms, suggested promising lines of research for future work, and generally contributed to our understanding of the processes maintaining intra-specific variation in natural populations at large

Camouflage chez les araignées crabe (approche sensorielle, comportementale et écologique)

Misumena vatia est supposée, depuis plus d un siècle, adapter sa couleur à celle de son substrat pour diminuer sa probabilité d être détectée par des proies et des prédateurs. Il existe cependant un décalage entre la quantité de travaux sur son écologie, sa notoriété en tant qu experte du camouflage, et la connaissance réelle sur son camouflage et le changement de couleur. Le but de cette thèse était d aborder le camouflage d un point de vue sensoriel, à une échelle communautaire, en combinant plusieurs approches. Il a été ainsi démontré que si M. vatia était indétectable dans l achromatique à longue distance, le niveau de contraste chromatique à courte distance était dépendant du substrat et de l identité du receveur. Des études électrophysiologiques et comportementales montrent de manière convergente que M. vatia possède la vision des couleurs. Les juvéniles utilisent cette habilité pour choisir des substrats qui les rendent peu détectable pour les proies. Enfin, les résultats de cette thèse sont replacés dans un contexte évolutif et physiologique plus général.Misumena vatia is assumed for more than a century to adapt its colouration to the colour of its substrate in order to decrease the risk of being detected by prey and predators. However, a discrepancy exists between the large quantity of works on its ecology, its fame as an expert of camouflage and the empirical knowledge about its cryspis and colour change mechanisms. The aim of this thesis was therefore to study crypsis from a community sensory perspective, using an approach combing physiology, behaviour and colour vision models. We showed that if M. vatia was undetectable at long distance through achromatic vision, the chromatic contrast value is quite dependent of both substrates and receiver identities. Electrophysiological recordings and behavioural choices all concur to show that M. vatia is able to see colours. Spiderlings use this ability for making choices among coloured backgrounds diminishing its conspicuousness to potential prey. Finally, the results of this thesis are discussed in an evolutionary and physiological context.TOURS-Bibl.électronique (372610011) / SudocSudocFranceF

The time-course of colour vision

Four experiments are presented, each investigating temporal properties of colour vision processing in human observers. The first experiment replicates and extends an experiment by Stromeyer et al. (1991). We look for a phase difference between combined temporal modulations in orthogonal directions in colour space, which might null the often-claimed latency of signals originating from the short-wavelength sensitive cones (S-cones). We provide another estimate of the magnitude of this latency, and give evidence to suggest that it originates early in the chromatic pathway, before signals from S-cones are combined with those that receive opposed L- and M-cone input. In the second experiment we adapt observers to two stimuli that are matched in the mean and amplitude of modulation they offer to the cone classes and to the cardinal opponent mechanisms, but that differ in chromatic appearance, and hence their modulation of later colour mechanisms. Chromatic discrimination thresholds after adaptation to these two stimuli differ along intermediate directions in colour space, and we argue that these differences reveal the adaptation response of central colour mechanisms. In the third experiment we demonstrate similar adaptation using the same stimuli, measured with reaction times rather than thresholds. In the final experiment, we measure the degree to which colour constancy is achieved as a function of time in a simulated stimulus environment in which the illuminant changes periodically. We find that perfect constancy is not achieved instantaneously after an illuminant chromaticity shift and that constancy of colour appearance judgements increases over several seconds

Change blindness: eradication of gestalt strategies

Arrays of eight, texture-defined rectangles were used as stimuli in a one-shot change blindness (CB) task where there was a 50% chance that one rectangle would change orientation between two successive presentations separated by an interval. CB was eliminated by cueing the target rectangle in the first stimulus, reduced by cueing in the interval and unaffected by cueing in the second presentation. This supports the idea that a representation was formed that persisted through the interval before being 'overwritten' by the second presentation (Landman et al, 2003 Vision Research 43149–164]. Another possibility is that participants used some kind of grouping or Gestalt strategy. To test this we changed the spatial position of the rectangles in the second presentation by shifting them along imaginary spokes (by ±1 degree) emanating from the central fixation point. There was no significant difference seen in performance between this and the standard task [F(1,4)=2.565, p=0.185]. This may suggest two things: (i) Gestalt grouping is not used as a strategy in these tasks, and (ii) it gives further weight to the argument that objects may be stored and retrieved from a pre-attentional store during this task

Anomalous trichromacy : external enhancement of colour signals, individual differences and diagnosis

Anomalous trichromacy is known to conceal a substantial range in perceptual ability, but this is not typically considered in assessments of corrective aids and diagnostic tests. In addition to the diversity caused by genetic polymorphisms, perceptual ability is thought to be influenced by little understood postreceptoral mechanisms, adding to the need for research focusing on this population. A modelling and behavioural investigation establishes the effectiveness of EnChroma filters in enhancing anomalous colour vision. Paper 1 (not yet published) employs a physiologically accurate model of colour vision to estimate the enhancements in cone-opponent signals conferred by the filters. Paper 2 (not yet published) presents behavioural validation of the model’s predictions, showing that notch filters can result in enhanced perceived saturation for deuteranomalous observers, with effects for suprathreshold perception and partial effects at absolute threshold. Paper 3 (submitted for publication) uses the physiologically accurate model of colour vision to investigate the impact of variation in edition and lighting conditions on the effectiveness of the Ishihara plates test in identifying those with mild anomalous trichromacy. The model predicts a significant impact of plate and illuminant, but no influence of edition, which is supported by the findings of a behavioural investigation. This thesis provides the first direct evidence that altering the input to the visual system using filter-based aids can impact the cone-opponent signals available to anomalous trichromats, and that this change in signal is useable by the visual system, resulting in changes to perceived saturatio

Language impairment and colour categories

Goldstein (1948) reported multiple cases of failure to categorise colours in patients that he termed amnesic or anomic aphasics. these patients have a particular difficulty in producing perceptual categories in the absence of other aphasic impairments. we hold that neuropsychological evidence supports the view that the task of colour categorisation is logically impossible without labels

The function and evolution of egg colour in birds

Animal colouration generally evolves via natural or sexual selection, or some combination of the two. From a naturalist‟s perspective, the diversity of colour exhibited by avian eggs is particularly interesting, because much of this diversity has not been thoroughly explained by either mode of selection. Until recently, a sexual selection mechanism for the evolution of egg colour was not known, and natural selection did not appear to be acting on some egg colours, most notably the unspotted white and blue-green eggs laid in open nests. The goal of my dissertation is to investigate the functional significance and selective pressures facing the evolution of egg colour. In Chapter 2, I investigate whether egg colour serves as signal of female quality. I find little support for this hypothesis and suggest that future research should examine other explanations for the evolution of egg colour. In Chapter 3, I find that environmental contaminants have a significant influence on egg colour. This has important implications for employing eggshell pigmentation as a non-destructive bio-indicator. In Chapters 4 and 5, I conduct large-scale comparative analyses that involve the reconstruction of a super-tree including representatives of all but one avian order. In Chapter 4, I find that predation is negatively related to ultraviolet chroma in open nests, and eggshell brightness is positively related to predation pressure in species using open nests above the ground. In addition, the risk of brood parasitism is greatest in species with a high proportion of blue-green chroma, but nest attendance is higher for these nests, suggesting that parents may behaviourally mitigate the risks of parasitism. I also find greater variation between clutches in species that experience high rates of parasitism; this presumably makes spotting a brood parasitic egg easier. In Chapter 5, I find that within cavity nests, selection is acting to increase eggshell brightness. I also find suggestive evidence that eggshell pigments could be adapted to protect the embryo from harmful solar radiation. In Chapter 6, I document and describe eggshell phosphorescence, a previously undocumented property, and suggest that this property is due to porphyrin within the eggshell

The contribution of colour to visual processing

The contribution that colour provides in visual object recognition was assessed in a variety of human and non-human primate species. A stimulus was designed to assess the degree to which removal of stimulus chromaticity affected object recognition ability. Stimuli were designed so that all chromatic modulation, all red-green chromatic modulation, all blue-yellow chromatic modulation or all achromatic modulation was removed. The stimuli were used in tests of object recognition to assess the functional advantage that stimulus colour or stimulus colour mediated by one of the chromatically opponent pathways provided towards object discrimination. Tests were carried out on normal human observers, macaque monkeys (Macca mulatta) and dichromatic marmoset monkeys (Callithrix jacchus). Experiments were conducted to examine the underlying neuronal processing of feature-like stimuli in visual area 1 (V1) of the anesthetised marmoset. Stimuli contained both chromatic and achromatic modulation or only achromatic modulation. Results showed that for all species, removal of stimulus chromaticity affected object recognition ability. For human observers and the macaque monkeys, the removal of red-green chromatic modulation impaired ability, the removal of blue-yellow chromatic information did not. Although cells were found in marmoset V1 that displayed selectivity for the feature-like elements used to construct the objects used in behavioural tests, they were rare. Few cells showed a significant response when stimuli contained chromaticity. It was concluded that stimulus chromaticity provides a functional advantage towards the sensory aspects of object recognition in humans, macaques and marmosets. For trichromatic species, there was a bias towards the red-green chromaticity providing a functional advantage. Although few cells were found to link the neural processes in V1 to these findings, V1 remains a candidate in the distributed map of neuro-anatomical areas that have been implicated in combining chromatic and achromatic cues to represent the visual world