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Of Mice and Fishes: Selection and the Maintenance of Variation Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2015 Of mice and fishes: selection and the maintenance of variation Lindholm, Anna K Abstract: Understanding how trait variation is maintained within populations is important for predict- ing how populations will respond to environmental change. This thesis uses observational, experimental, modelling, population and quantitative genetic approaches to investigate proximate and ultimate mech- anisms underlying the maintenance of variation in two species of fishes and mice. One important feature unites these four species: they can be observed and captured in the wild, and they can be kept in the laboratory and subjected to controlled experiments. The three conditions under which natural selection can maintain within-population variation were investigated: 1) variants have equal fitness, 2) selection eliminates variation but new variants are continuously generated, and 3) a balance of selective forces. Most of the work here described investigates the latter. Evidence was found for temporal fluctuation in selection in striped mice Rhabdomys pomilio (Chapter 3) and in guppies Poecilia reticulata (Chapter 8), and spatial fluctuation in selection in guppies (Chapter 7) from introduced populations (Chapter 5). We considered negative frequency-dependent selection as a mechanism to maintain rare male colour morphs in Poecilia parae (Chapter 1) and Major Histocompatibility Complex allelic variation in house mice Mus musculus domesticus (Chapter 10). Chapters 10 and 11 investigate selection at different levels at the t haplotype, which is a driving selfish genetic element in house mice. While the t haplotype has an advantage relative to the wildtype allele in transmission to the next generation, thereby experiencing positive selection, it is selected against at the level of the animal because homozygotes die prenatally. However, female heterozygotes do have a survival benefit through heterosis (Chapter 11) and Chapter 12 tests whether this survival difference between genotypes has correlated behavioural effects. Genetic tools to facilitate estimates of selection were developed in Chapter 14. Whether selection influences trait vari- ation in the next generation depends on their proximate bases. Proximate genetic bases of trait variation were investigated in Chapters 1,2, 6 and 15 while proximate environmental bases of trait variation were considered in Chapters 3, 4, 8, 9 and 13. The combination of understanding patterns of selection and the additive genetic versus environmental contributions to trait variation are important in predicting how populations will respond to the environmental challenges of tomorrow. Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-108645 Habilitation Published Version Originally published at: Lindholm, Anna K. Of mice and fishes: selection and the maintenance of variation. 2015, University of Zurich, Faculty of Science. Of mice and fishes: selection and the maintenance of variation Habilitationsschrift zur Erlangung der Venia legendi für Verhaltensbiologie und Evolutionsbiologie an der Mathematisch‐naturwissenschaflichen Fakultät der Universität Zürich Anna Lindholm Oberassistentin am Institut für Evolutionsbiologie und Umweltwissenschaften Zürich, Dezember 2013 Contents Introduction ............................................................................................................................................. 3 Summary ............................................................................................................................................... 14 Acknowledgments ................................................................................................................................. 15 References ............................................................................................................................................. 16 Chapter 1 Extreme polymorphism in a Y-linked sexually selected trait .............................................. 18 Chapter 2 Sex chromosomes and sexual selection in poeciliid fishes ................................................. 26 Chapter 3 Relative fitness of alternative male reproductive tactics in a mammal varies between years ...................................................................................................................................................... 38 Chapter 4 Social flexibility and social evolution in mammals: a case study of the African striped mouse (Rhabdomys pumilio) ................................................................................................................. 49 Chapter 5 Invasion success and genetic diversity of introduced populations of guppies Poecilia reticulata in Australia ............................................................................................................................ 63 Chapter 6 Where do all the maternal effects go? Variation in offspring body size throughout ontogeny in the live-bearing fish Poecilia parae ................................................................................... 76 Chapter 7 Causes of male sexual trait divergence in introduced populations of guppies .................. 81 Chapter 8 Environmental variation and the maintenance of polymorphism: The effect of ambient light spectrum on mating behaviour and sexual selection in guppies .................................................. 97 Chapter 9 The complex social environment of female house mice (Mus musculus domesticus) ..... 108 Chapter 10 Mate choice for genetic compatibility in the house mouse ............................................ 130 Chapter 11 Polyandry and the decrease of a selfish genetic element in a wild house mouse population ........................................................................................................................................... 149 Chapter 12 A selfish genetic element influencing longevity correlates with reactive behavioural traits in female house mice (Mus domesticus) ............................................................................................. 169 Chapter 13 The nasty neighbour in the striped mouse (Rhabdomys pumilio) steals paternity and elicits aggression ................................................................................................................................. 179 Chapter 14 Development of polymorphic microsatellite markers for the livebearing fish Poecilia parae ................................................................................................................................................... 188 Chapter 15 Direct selection on male attractiveness and female preference fails to produce a response .............................................................................................................................................. 193 2 Introduction About nine million species inhabit the Earth (MORA et al. 2011). Within species individuals typically vary in their characteristics, thus the living world is composed of an uncountable diversity of forms. Understanding how this came to be and will change in the future are the main challenges of the field of evolutionary biology. The aim of this thesis is to investigate how contemporary variation is maintained, using two mammal and two fish species, and different kinds of traits. Variation occurs at the genetic and phenotypic level. What is often measured is phenotypic variation, which is variation in observable characters that result from the interaction between genes and the environment in which they are expressed. For example, males of some species of live‐bearing poeciliid fishes show impressive phenotypic variation in colour pattern, and also in body size (Figure 1). These are not local adaptations, with a single well‐ adapted colour pattern per population, as all occur together within populations in the same habitat. How can this be explained? There are two types of answers, one based on proximate causes (mechanisms) and one on ultimate causes (current adaptation and evolutionary history). G Figure 1. A‐E. Phenotypic variation in male Poecilia parae within a natural population. F. Female P. parae. Source: Chapter 1. G. Phenotypic variation in male guppies P. reticulata from a single feral population in Australia. In poeciliid fishes, proximate causes of colour pattern variation are differential distribution of pigment cells with different absorbance spectra in the skin (BLANCHARD et al. 1991). Pigmentation variation in this family of fishes is mainly the result of genetic differences between individuals at autosomes, X and Y chromosomes (Chapter 2) but is also modulated by environmental differences, such as carotenoid content of the diet (GRETHER et al. 1999). 3 Male‐specific colour patterns are under hormonal control and develop near sexual maturity (HOUDE 1997). Ultimate causes of colour pattern variation relate to current and historical patterns of natural selection. Natural selection is the process in which alleles change in frequency between generations depending on the relative survival and reproductive success of organisms bearing those alleles. In the case of Poecilia parae, the less spectacularly coloured morphs (to our eyes) make up a high proportion of adult males within populations (Chapter 1), and the high frequency indicates that these morphs must have a selective advantage. Subsequent research has
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