University of Illinois Urbana-Champaign

The maintenance of variation in Cyprinodontiformes

Johnson, Ashley

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Ashley_Johnson.pdf

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https://hdl.handle.net/2142/42447

Description

Title
The maintenance of variation in Cyprinodontiformes
Author(s)
Johnson, Ashley
Issue Date
2013-02-03T19:45:55Z
Director of Research (if dissertation) or Advisor (if thesis)
Fuller, Rebecca C.
Doctoral Committee Chair(s)
Fuller, Rebecca C.
Committee Member(s)
  • Cáceres, Carla E.
  • Robinson, Gene E.
  • Hughes, Kimberly A.
Department of Study
School of Integrative Biology
Discipline
Biology
Degree Granting Institution
University of Illinois at Urbana-Champaign
Degree Name
Ph.D.
Degree Level
Dissertation
Date of Ingest
2013-02-03T19:45:55Z
Keyword(s)
  • color variation
  • Lucania goodei
  • Poecilia reticulata
  • carotenoid
  • pterin
  • Melanin
  • opsin
Abstract
Maintenance of genetic variation in the face of strong natural selection is a long-standing problem in evolutionary biology. Two extreme examples of this are the guppy (Poecilia reticulata) and the bluefin killifish (Lucania goodei), two freshwater species in the order Cyprinodontiformes with extensive within-population color pattern variation found among males. I use these two species as case studies to examine the evolution and maintenance of color pattern variation. First, I examine a potential reason behind the evolution of a female mating preference for males with novel color patterns in guppies. This preference has been implicated as a factor in maintaining the genetically-determined color pattern polymorphisms found in male guppies, and inbreeding avoidance has been proposed as a mechanism to explain its evolution. Inbreeding avoidance is advantageous when populations exhibit inbreeding depression and the opportunity for mating between relatives exists. To determine whether these conditions are met in a natural guppy population, I assessed mating and reproductive patterns using parentage analysis. Females produced more offspring with less-related males than with more-related ones. In addition, females were more likely to have mated with less-related males, but this trend was only marginally significant. Male heterozygosity was positively correlated with mating success and with the number of offspring sired, consistent with strong inbreeding depression for adult male fitness. These results show that strong inbreeding depression occurs in guppies, and individuals tend to avoid mating with relatives. Thus, the preference for novel male phenotypes may have evolved due to the advantage inherent to avoiding inbreeding. In my remaining chapters, I focus the bluefin killifish (Lucania goodei). These fish exhibit extensive color variation in their fins, but the function of this variation has not yet been determined. I collected males from multiple populations across Florida and used absorption spectroscopy to identify the pigments responsible for the fin coloration. I determined that orange coloration in the caudal fin was caused by a carotenoid pigment. Color in the anal fin was either pterin based (yellow and red) or structural (blue) with a melanic fin border. Using a behavioral assay designed to measure dominance, I sought to determine the informational content of each pigment. Black melanic markings on the anal fin were strongly related to dominance. Aggression was greater between males of similar sized melanic stripes, indicating that they functioned as badges of status in territorial interactions with other males. In keeping with their dietary origin, caudal carotenoid levels positively correlated with condition but did not influence dominance interactions. However, the highly labile ornament predicted parasite infection and spawning success, suggesting a role in intersexual selection, with caudal carotenoid as a signal of health to potential mates. Similarly, pterin pigmentation in the anal fin, while not related to dominance, was related to overall spawning levels and parasite infection, suggesting that pterin pigmentation may also signal immune status. In order to test whether the variation found in fin color has effects on fitness, I set up a breeding experiment in which I examined the role of the anal fin polymorphism and the amount of pterin, melanin, and carotenoid pigmentation in each male. I manipulated anal fin morph ratios in breeding populations housed in a greenhouse to determine if morph rarity conferred a fitness advantage, as determined by identifying fry paternity. I found no evidence of negative frequency-dependent selection on anal fin morph. However, red morph males did sire more offspring on bottom spawning substrates when rare. This suggests lighting environment may affect female preference and influence morph abundance. In addition to noting morph effects, I also tested the effects of level of pigmentation on male fitness. I demonstrated that males with more anal fin pigmentation (both pterin and melanin) and caudal fin pigmentation (carotenoid) sired more offspring. Finally, I examined the interplay of lighting environment, visual system oscillations, and color preferences in Lucania goodei. I measured the diurnal pattern of cone opsin gene expression in the bluefin killifish to see if overall or proportional opsin expression was tuned to match the daily blue-shift in light at dawn and dusk. LWS, RH2-1, RH2-2, and SWS2B (but not SWS1 or SWS2A) opsin gene expression was lowest at midnight and dawn and highest at midday and dusk, and the observed temporal shifts were many times larger than an accompanying difference in production of opsins in tannin-stained versus clear water habitats. I also measured color preference in a foraging assay at dawn, midday, and dusk to determine if opsin gene expression influenced fish behavior. Rather than correlating with opsin expression, foraging behavior matched lighting conditions, with higher preferences for blue at noon and red at dawn/dusk, when these wavelengths are comparatively scarce and the contrast of these colors is increased. My results suggest that L. goodei exhibit strong diurnal cycles of opsin expression but that these are not correlated with light intensity or light color per say. Temporally variable preferences for different colors are probably the result of lighting environment rather than opsin production. The results from the studies on Lucania goodei suggest that the color pattern variation observed in this species is affected by several factors. The continuous variation found in degree of pigmentation (anal fin melanin, anal fin pterin, and caudal fin carotenoid) reflect variation in condition or fighting ability. In contrast, lighting environment may strongly influence the red/yellow/blue polymorphism found in the anal fin. When red wavelengths are rare, as at dawn and dusk and in deep waters, red males may have a mating advantage over blue and yellow males. When blue wavelengths are rare, as in tannin-stained waters and at noon, blue males may have a mating advantage. Thus, temporal and microhabitat variation may contribute to the maintenance of the anal fin polymorphism.
Graduation Semester
2012-12
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http://hdl.handle.net/2142/42447
Copyright and License Information
Copyright 2012 Ashley Johnson

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