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Title:Behavioral and genomic patterns of evolution during speciation via reproductive and agonistic character displacement
Author(s):Moran, Rachel Lynn
Director of Research:Fuller, Rebecca C.
Doctoral Committee Chair(s):Fuller, Rebecca C.
Doctoral Committee Member(s):Bell, Alison M.; Berlocher, Stewart H.; Mendelson, Tamra C
Department / Program:School of Integrative Biology
Discipline:Ecol, Evol, Conservation Biol
Degree Granting Institution:University of Illinois at Urbana-Champaign
Subject(s):Speciation, reinforcement, hybridization, character displacement
Abstract:Interspecific reproductive interactions, such as hybridization or fighting over access to mates, are surprisingly common given that they frequently result in negative fitness consequences. Selection to avoid hybridizing with another species can result in mating trait evolution via reproductive character displacement (RCD). Similarly, selection to avoid aggressive interactions with another species can result in agonistic character displacement (ACD). Both RCD and ACD can lead to a pattern of enhanced preferences for mating or fighting with conspecifics over heterospecifics in areas of sympatry compared to allopatry. Behavioral isolation can potentially evolve among populations within a species as a correlated effect of RCD or ACD, termed cascade RCD (CRCD) or cascade ACD (CACD). My dissertation research integrated behavioral and genomic approaches to investigate the role of character displacement in promoting speciation in a diverse clade of stream fishes called darters (Percidae: Etheostominae). I focused on two groups in the subgenus Oligocephalus: the orangethroat darters clade (Etheostoma: Ceasia) and the rainbow darter (Etheostoma caeruleum). I found behavioral evidence for male-driven RCD and ACD between multiple orangethroat species and their respective sympatric rainbow darter populations. When orangethroat and rainbow darters occur sympatrically, males prefer conspecific over heterospecific females and bias their aggression towards conspecific over heterospecific males. Such preferences are absent when these species occur allopatrically. I also found that RCD and ACD between orangethroat and rainbow darters has secondarily caused mating and agonistic traits to diverge among orangethroat lineages. When orangethroat species occur in sympatry with rainbow darters, orangethroat males preferentially mate and fight with conspecifics over another closely related orangethroat species. However, when orangethroat species are allopatric with respect to rainbow darters, orangethroat males do not differentiate between conspecific versus heterospecific orangethroat males and females. This is consistent with both CRCD and CACD within the orangethroat darter clade and represents the only known example of CACD to date. Notably, females do not exhibit preferences for variable components of male coloration between or within species, despite the presence of sexual dimorphism and traditional sex roles. Instead, color pattern functions in male competition. I found that male color pattern is more divergent between orangethroat and rainbow darters in sympatry versus allopatry. Consequently, males bias aggression towards conspecific over heterospecific males in sympatry but not in allopatry. This shows that male competition alone can lead to color pattern divergence between and within species via ACD and CACD. The failure to detect female mate preferences in this system may be due to females facing a high cost to choosiness, as I observed that egg viability decreases rapidly with time since ovulation. Together, these results contradict the classic paradigm that female preference promotes the evolution of behavioral isolation in species where males exhibit elaborate secondary sex traits. Selection to avoid hybridization has likely promoted the evolution of RCD and ACD between orangethroat and rainbow darters. I used genomic data to show that hybridization is ongoing and that backcross hybrids suffer high mortality. To investigate the genetic mechanisms underlying postzygotic isolation between these species, I assembled the orangethroat darter genome and transcriptome, resulting in the first annotated darter draft genome. I also generated linkage maps for orangethroat and rainbow darters. Using these tools, I identified several putative chromosomal translocations that may be implicated in genetic incompatibilities. Analyses of restriction-site associated DNA sequencing (RADseq) data in laboratory-generated backcross hybrids revealed strong selection against recombinant individuals. This represents one of the few studies to use fine-scale ancestry mapping in hybrids to characterize genome-wide patterns corresponding to genetic incompatibilities in non-model species. My results indicate that a large proportion of the genome is involved in postzygotic isolation, which in turn (1) directly promotes RCD/ACD in sympatry between orangethroat and rainbow darters and (2) indirectly promotes CRCD/CACD among orangethroat darter lineages. Overall, my dissertation research has significantly changed our understanding of speciation in darters and has provided novel insight into the genomic architecture of hybrid incompatibilities that promote character displacement. The genomic resources that I generated for my dissertation research will undoubtedly serve as valuable tools for future studies on speciation, sexual selection, phylogenetics, mating system evolution, and conservation in darters.
Issue Date:2019-04-09
Rights Information:Copyright 2019 Rachel Moran
Date Available in IDEALS:2019-08-23
Date Deposited:2019-05

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