The descent of damselflies and variation in relation to sex

Sexual conflict over mating shapes the interactions between males and females in many animals and is also responsible for dramatic adaptations in both sexes. In some species of pond damselflies (Odonata:Coeangrionidae), sexual conflict maintains discrete female-limited colour morphs over multiple generations and within populations. One of the female morphs is typically male-coloured and considered a male mimic. This is because their male-like appearance provides a frequency-dependent advantage against excessive male mating attempts. In this thesis, I investigate three major questions regarding the evolutionary consequences of this pervasive sexual conflict. First, how is phenotypic variation in ecological traits distributed among heritable female colour morphs? Second, how does sexual conflict shape phenotypic variation within the lifespan of females? Finally, how, where and why do female-limited morphs arise in the first place?
In the Common Bluetail damselfly (Ischnura elegans), female morphs differ in multiple phenotypic traits. My results uncover further phenotypic associations between the two most common morphs of the Common Bluetail in Sweden. One morph is more resistant to infections by parasitic mites, whereas the other is instead more tolerant. These morphs also differ in their developmental sensitivity to temperature, which in turn influences how morph frequencies are distributed across European populations. Moreover, my findings provide some insights as to how these profound phenotypic differences are produced over the course of adult development, and suggest that male mimics and non-mimics differ in the regulation of important developmental processes.
Females of the Common Bluetail undergo dramatic colour changes as they become sexually mature. My thesis shows that immature colour patterns in non-mimic female morphs reduce male pre-mating harassment, and may have evolved by co-opting male colour signals to be expressed as immature signals of reproductive unsuitability. These results suggest that female colour patterns might be highly evolutionarily labile. Yet, a large-scale phylogenetic framework is required to gain a full understanding of the macroevolutionary consequences of sexual conflict on the evolution of female-limited colour variation.
I inferred a multi-locus phylogeny for the damselfly superfamily Coeangrionoidea. I then used this phylogeny to show that female-limited colour polymorphisms have arisen repeatedly in this clade, and in association with ecological conditions that foster sexual conflict over mating. Finally, my results uncover a stark contrast between the consequences of sexual conflict at micro and macroevolutionary scales. While sexual conflict promotes diversity within populations by maintaining alternative female morphs, the presence of these morphs is also associated with increased extinction risk and a fast lineage turnover. Together, my results reveal how sexual conflict can influence the origin, distribution and loss of diversity.

We are lucky to live in a changing world, and with change comes variation. The immense variation in the external features of animals, and particularly their colour, fascinates scientists and non-scientists alike. In this thesis, I explore several aspects of why and how colour variation evolves in a charismatic group of insects. Pond damselflies are colourful, diurnal and visually driven organisms. Males use their vision to find females with whom they will attempt to mate. Females, however, would often fare better without excessive male attention, which reduces their fecundity. This fundamental conflict between the sexes arises because, as in many other animal species, damselfly females invest more time and energy in each of their offspring than males do, hence their reproductive success does not require access to many males. In contrast, it is in the best interest of males to mate with multiple females. My research has dealt with the consequences of this form of sexual conflict for the evolution of pervasive female diversification.
In some species of damselflies, females, but not males, occur in discrete colour morphs. These female morphs have remarkably different colour patterns and there are no intermediates. In fact, as far as we know, a single gene determines whether a female develops into one colour morph or another. My research shows that these female-limited colour polymorphisms have evolved repeatedly and independently over the nearly 40 million-year history of pond damselflies. Moreover, female colour morphs arise in damselflies under ecological conditions that promote conflict between females and males. This occurs, for instance, when many adult individuals are confined to a restricted breeding area and have a short time window of opportunities to mate.
One of the female morphs in pond damselflies is typically a male mimic, which avoids potentially harmful male-mating attempts due to its resemblance to males. A statistical reconstruction of the ancestral history of pond damselflies showed that when female-limited colour polymorphisms evolve, it is due to the origin of a new male-mimicking morph, in an ancestral species where males and females looked different from each other. This further suggests that sexual conflict is the major cause for the evolution of multiple female morphs. For females, however, the risks of unsought male persistence start early, before they are even capable of reproduction. The results of my thesis also suggest that male-like colour signals have evolved repeatedly among females that are not male mimics, but these females only display such colour patterns when they are sexually immature. These immature colour signals also discourage males from approaching females.
Are there any consequences of the evolution of female colour morphs, beyond the interactions between the sexes? This thesis, along with previous studies, also shows that female morphs differ in a variety of other characteristics that influence female survival and reproduction. My research provides evidence that the gene that controls morph determination influences many other genes during the course of female development. In one particular species, the Common Bluetail, these gene interactions may underlie the differentiation between male-mimics and non-mimics in the timing of several important developmental events. Moreover, these interactions have consequences for the performance of females in different external environments. I show that the two most common morphs in the Common Bluetail in Sweden, differ in their defence strategies against parasitic water mites. One morph does better at fending off the mites, whereas the other sees its reproduction nearly unaffected by mite infections.
If male-mimicking females can avoid some male harm with their appearance, one may ask, why are not all females mimicking males? The answer is that the benefits of male mimicry are reduced as the male mimics become more common in a population. Under such conditions, males might be less prone to fall for their deceit and alternative female morphs, which are now off-target, may thrive. This is why, within populations, sexual conflict can maintain female-limited colour variation over long periods of time, as the fates of the alternative morphs cycle through generations. However, over even longer time scales, sexual conflict may have very different consequences. I found that the evolution of multiple female morphs is also associated with a higher extinction risk. Sexual conflict can therefore have profound effects on many of the characteristics of animal species and influence the origin, maintenance and loss of their diversity.