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Evolution of Male Coloration in The Wild: The Role of Sex Linkage and Selection

  • Author(s): Gordon, Swanne Pamela
  • Advisor(s): Reznick, David
  • et al.

Male secondary sexual characters can be quite distinct, striking, and elaborate in nature. Despite many advances in the field of sexual selection, much remains to be known regarding why some organisms evolve these features more than others. Since Darwin published On the Origin of Species in 1859, many studies have measured the strength of natural selection in the wild showing that it is often strong and rapid (Both and Visser 2001; Pelletier et al. 2007; Kinnison et al. 2008; reviews: Hendry and Kinnison 1999; Reznick and Ghalambor 2001; Stockwell et al. 2003; Strauss et al. 2008; reviews: Endler 1986; Kingsolver et al. 2001; Hairston Jr. et al. 2005). Despite all these examples, a recent review has shown that very few of the traits measured in these studies involve secondary selected traits (Svensson and Gosden 2007). This is unfortunate because secondary selected traits often represent the most complex, elaborate traits in a variety of taxa including plants (eg. Geber, Dawson, and Delph 1998), insects (ex. Stubblefield and Seger 1994), fish (eg. Basolo and Trainor 2002), birds (eg. Hill and McGraw 2006), and reptiles (eg. Schulte-Hostedde and Schank 2009). Moreover, the evolution of one these particular traits in nature, male guppy coloration, represents one of our best examples of rapid evolution (Endler 1980).

Adaptation requires both inheritance and selection, however most studies in rapid evolution either ignore heritability and concentrate on selective pressures or assume a particular mode of inheritance. Theoretical models have long established the importance of genetic architecture through sex linkage in sex-limited or sexually selected traits. However, empirical research in this topic is rare. In this thesis I present a comprehensive experimental study of how ecology and sex-linkage may interact to maintain the genetic variation and complex polymorphism in a sexually antagonistic, sex-limited trait in the wild.

First I use a standard multivariate animal model to evaluate the heritability of two sub-traits of male coloration known to be linked to male fitness; orange and black body coloration. I also partition phenotypic variance of two introduced populations of guppies Poecilia reticulata) into its environmental and genetic components. The genetic components are then further partitioned into Y-linked versus non Y-linked variance to test the idea that sexually selected male traits are generally linked to the Y-chromosome where evolution is presumed to be faster as established by theory. I also studied genetic correlations among the two color patterns, and use all findings to predict the future trend of evolutionary change in this novel introduction. Using a quantitative genetics approach in this manner can help extract the genetic parameters affecting evolutionary change, and to my knowledge is the first study that separates Y-linked from non Y-linked quantitative genetic variance using a wild pedigree. Results show high proportion of Y-linked to non-Y linked genetic variance and that overall variation in Y-linkage accounts for most of the phenotypic variation in both introduction sites. Both sub-traits are also highly heritable and so combined with the abrupt change in selection pressure with the introduction I predict evolutionary change to be rapid in these populations.

Second, following the results garnered in Chapter 1, here I track changes in adaptive divergence in both introduction sites bimonthly for one year post-introduction to see if our predictions were sound. My goal in this chapter was to investigate how variation in different selective pressures, such as predation and stream canopy cover, affect rates of divergence in a sexually selected polymorphic trait. Guppies were introduced from environments where they coexist with predators to two novel environments where there are no predators. In addition to the abrupt change in predation pressure, I also manipulated the canopy cover in one introduction site, hence doubling productivity in that environment. Results show rapid phenotypic and genotypic divergence in male coloration as expected, to date the fastest measure of change in wild guppies. Results also demonstrate that abrupt changes in habitat as well as predation-mediated mortality rates affect variation in rates of evolution of secondary sexual characters, an idea previously proposed but never formally tested.

In the third Chapter I test the idea that microgeographic variation in sex-linkage occurs in multiple high- versus low-predation guppy populations, the first step needed to test theory regarding interactions between sex-linkage and selection. I examine a hypothesis that high-predation guppies have mainly Y-linkage of color patterns whereas low-predation guppies have color patterns linked to both the X- and Y-chromosome. In my thesis chapter I examine multiple high- and low-predation natural population using hormone assays in female guppies (which normally do not show coloration, and do not have a Y-chromosome) to test for differences in X-/autosomal linkage. I presume that changes in the amount of non-Y linked inheritance are combined with changes in Y-linkage. I also examine three introduction populations (from high- introduced into low predation sites) to see if these differences in linkage relationship respond rapidly to selection pressure. Results show that indeed low-predation guppies show a significantly higher amount of non-Y linked color patterns compared to high-predation guppies, and that this variation in linkage relationship can evolve in a matter of few guppy generations.

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