Colour vision of Ischnura heterosticta (Insecta: Odonata): Role in sexual selection, communication and visual plasticity

Abstract

Sensory systems are important for any life task of an animal. Vision, and colour vision in particular, is essential for visual–based insects, such as Odonata (damselflies and dragonflies), many of which display colour patterns on their bodies. Numerous behavioural studies suggest that the diverse colour patterns function as a means for intersexual, intrasexual, interspecific, or intraspecific recognition and play a role in sexual selection, particularly in ischnuran damselflies that have sex-limited polymorphism. However, to date there are no comprehensive studies linking behavioural to electrophysiological evidence to support the role of colour patterns and colour vision in mate choice in this group of insects. In my Ph.D. thesis, I investigated the function of body colouration and colour vision in sexual selection and communication of the Australian polymorphic damselfly, Ischnura heterosticta, and examined the mechanisms underlying its colour vision and colour discrimination ability. In an observational study (Chapter 2), I surveyed I. heterosticta reproductive behaviours and daily activity patterns in the field, providing the first detailed account of their colour morphs and behavioural biology. Andromorph females are blue like males, and gynomorph females have colour morphs in green, intermediate, and grey. Mating pairs, usually with gynomorphs, are formed after dawn and mating can last up to 3-4 hours. Oviposition occurs in the days after mating, and ovipositing females are subjected to aggressive male harassment, which varies with female colouration. These data provided the biological foundation regarding colour-based sexual selection in I. heterosticta investigated in the following chapters. In the next set of experiments (Chapter 3), I discovered a unique irreversible ontogenetic colour change in females of I. heterosticta: blue andromorphs are sexually immature individuals that emerge from nymphs. After 4 to 7 days, they turn into green-grey gynomorphs to signal their sexual maturity and advertise readiness to mate. Gynomorphs are the preferred mating partners, which suggests that blue andromorphs avoid unnecessary long mating during sexual immaturity through their male-mimicking colouration. This discovery provided the first indication that colour plays a key role in mate choice and that female polymorphism in I. heterosticta may be maintained via colour signals. In the next study (Chapter 4), I tested whether and how male mating preference was associated with colour cues by manipulating female body colours artificially. The outcomes strongly suggest that female body colouration is the key visual signal for mate choice in I. heterosticta. Males always preferred gynomorph females irrespective of female ratio or prior mating experience. Only under low ambient light males of I. heterosticta occasionally misidentified blue andromorphs as mating partners, likely as consequence of the insufficient light. This finding provided the behavioural indication that ischnuran damselflies rely on colour vision for mate recognition. The next study (Chapter 5) examined the morphological structure of the compound eyes of I. heterosticta using histological approaches. The diameter of an ommatidium is about 10 μm, and its length can be up to 400 μm depending on the area of the retina. Several retinula cells were identified distributed along the ommatidium. This provided essential background information on the visual anatomy in this species, and the anatomical indication that I. heterosticta may have colour vision, which was investigated in the next chapter. I used electrophysiological approaches (Chapter 6) to investigate the spectral sensitivities of the visual system of I. heterosticta. The results showed that they have trichromatic vision, being able to detect UV, blue and green light. Contrast calculations confirmed that their colour discrimination ability enables them to distinguish the spectral differences of individual female morphs. These results were congruent with the behavioural findings from previous chapters, showing that I. heterosticta use colour signals for mate choice in context of sexual selection. The final study (Chapter 7) examined the molecular basis of colour vision in I. heterosticta, and investigated whether it is plastic and dependent on light experience. I identified three types of opsin genes in I. heterosticta, corresponding to three wavelengths of light (UV, blue and green), confirming that this species is trichromatic. I found that during development opsins are differentially expressed in nymphs (aquatic) and adults (terrestrial/aerial), and opsin expression also changes when individuals are reared or kept under different ambient light conditions. These findings were further supported by electrophysiological experiments, showing an equivalent change in response. This demonstrates that colour vision in I. heterosticta is plastic and that ambient light induces visual plasticity. This plasticity facilitates adaptation to the changing visual environments during development, and ensures that adults can detect the crucial colour cues that are key for mate choice and reproduction. This thesis is the first comprehensive study examining the functional role of colour vision and body colouration in a polymorphic ischnuran damselfly. This body of work also contributes important new insights into the mechanisms underlying sexual selection, evolution and maintenance of female-limited polymorphism in I. heterosticta.