Articles & Supporting Data

Permanent link for this collectionhttps://hdl.handle.net/2022/16818

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Adaptation, Exaptation, and Constraint: A Hormonal Perspective
(American Society of Naturalists, 1999-07) Ketterson, Ellen D.; Nolan, Val Jr
We approach conceptual issues in evolutionary biology from an endocrinological perspective, noting that single hormones typically act on several target tissues and thereby mediate suites of correlated phenotypic traits. When several components of such a suite are beneficial, an important evolutionary question is whether all are adaptations or some are exaptations. The answer may depend on whether the traits arose in response to selection on variation in systemic levels of the hormone on variation in responsiveness of target tissues to invariant levels of the hormone. If the former, selection probably acted directly on fewer than all traits; beneficial traits arising indirectly would be exaptations. In contrast, multiple beneficial traits that arose out of independent changes in target‐tissue sensitivity to invariant hormone levels could all be adaptations. Knowledge of specific hormonal mechanisms as well as of historical selective regimes will be necessary to draw such distinctions. Endocrine constraints on evolution can be studied experimentally by applying hormones systemically and measuring interdependent responses of beneficial and detrimental traits to selection (phenotypic engineering with hormones). Supposing that alteration of one trait in isolation would enhance fitness, cases in which the net effect of endocrine alteration of multiple traits is to depress fitness provide evidence for constraints. We briefly report results of recent studies employing hormonal manipulations, stressing our own work on the dark‐eyed junco (Junco hyemalis: Emberizidae).
Testosterone and Avian Life Histories: Effects of Experimentally Elevated Testosterone on Behavior and Correlates of Fitness in the Dark-Eyed Junco (Junco hyemalis)
(American Society of Naturalists, 1992-12) Ketterson, Ellen D.; Nolan, Val Jr; Wolf, Licia; Ziegenfus, Charles
Hormones influence many aspects of organismal behavior, physiology, and morphol- ogy, and thus hormones may lie at the root of many life-history trade-offs. By manipulating hormones we can create novel phenotypes (i.e., perform phenotypic engineering) and attempt to relate phenotypic variation to fitness. We report the effect of testosterone treatment on parental behavior and vocal behavior of adult male dark-eyed juncos. Testosterone partially suppressed paternal behavior and increased the frequency of song. When we compared treated males and controls for nine potential correlates of fitness (offspring growth and survival to the age of 10 d, condition of females, length of the interval between consecutive nestings, size of subsequent clutches and broods, mate retention within and between breeding seasons, and survival rate), we found no statistical differences. In some measures treated males outperformed controls, but in most the reverse was true. The power of some of our tests was not great enough to detect small differences. At this stage of our investigation, three interpretations of our results seem almost equally probable: (1) a broad range of behavioral phenotypes is selectively neutral in the junco, (2) male parental behavior is beneficial to males only in some years or habitats, or (3) we have yet to measure the correlates of fitness that are most strongly affected by the behavioral changes induced by elevated testosterone
Hormones and Life Histories: An Integrative Approach
(American Society of Naturalists, 1992-11) Ketterson, Ellen D.; Nolan, Val Jr
Because of their role in mediating life‐history trade‐offs, hormones are expected to be strongly associated with components of fitness; however, few studies have examined how natural selection acts on hormonal variation in the wild. In a songbird, the dark‐eyed junco (Junco hyemalis), field experiments have shown that exogenous testosterone alters individuals’ resolution of the survival‐reproduction trade‐off, enhancing reproduction at the expense of survival. Here we used standardized injections of gonadotropin‐releasing hormone (GnRH) to assay variation in the testosterone production of males. Using measurements of annual survival and reproduction, we found evidence of strong natural selection acting on GnRH‐induced increases in testosterone. Opposite to what would be predicted from the survival‐reproduction trade‐off, patterns of selection via survival and reproduction were remarkably similar. Males with GnRH‐induced testosterone production levels that were slightly above the population mean were more likely to survive and also produced more offspring, leading to strong stabilizing selection. Partitioning reproduction into separate components revealed positive directional selection via within‐pair siring success and stabilizing selection via extrapair mating success. Our data represent the most complete demonstration of natural selection on hormones via multiple fitness components, and they complement previous experiments to illuminate testosterone’s role in the evolution of life‐history trade‐offs.
Natural Selection on Testosterone Production in a Wild Songbird Population
(The American Naturalist, 2010-04-15) McGlothlin, Joel W.; Whittaker, Danielle J.; Schrock, Sara E.; Gerlach, Nicole M.; Jawor, Jodie M.; Snajdr, Eric A.; Ketterson, Ellen D.
Because of their role in mediating life‐history trade‐offs, hormones are expected to be strongly associated with components of fitness; however, few studies have examined how natural selection acts on hormonal variation in the wild. In a songbird, the dark‐eyed junco (Junco hyemalis), field experiments have shown that exogenous testosterone alters individuals’ resolution of the survival‐reproduction trade‐off, enhancing reproduction at the expense of survival. Here we used standardized injections of gonadotropin‐releasing hormone (GnRH) to assay variation in the testosterone production of males. Using measurements of annual survival and reproduction, we found evidence of strong natural selection acting on GnRH‐induced increases in testosterone. Opposite to what would be predicted from the survival‐reproduction trade‐off, patterns of selection via survival and reproduction were remarkably similar. Males with GnRH‐induced testosterone production levels that were slightly above the population mean were more likely to survive and also produced more offspring, leading to strong stabilizing selection. Partitioning reproduction into separate components revealed positive directional selection via within‐pair siring success and stabilizing selection via extrapair mating success. Our data represent the most complete demonstration of natural selection on hormones via multiple fitness components, and they complement previous experiments to illuminate testosterone’s role in the evolution of life‐history trade‐offs.
Deciphering Information Encoded in Birdsong: Male Songbirds with Fertile Mates Respond Most Strongly to Complex, Low-Amplitude Songs Used in Courtship
(The American Naturalist, 2011-08-15) Reichard, Dustin G.; Rice, Rebecca J.; Vanderbilt, Carla C.; Ketterson, Ellen D.
Research on the function of acoustic signals has focused on high-amplitude long-range songs (LRS) and largely ignored low-amplitude songs produced by many species during close-proximity, conspecific interactions. Low-amplitude songs can be structurally identical to LRS (soft LRS), or they can be widely divergent, sharing few spectral and temporal attributes with LRS (short-range song [SRS]). SRS is often more complex than LRS and is frequently sung by males during courtship. To assess function, we performed two playback experiments on males of a socially monogamous songbird. We compared responses of males whose mates were fertile or nonfertile with differences in song structure (SRS vs. LRS and soft LRS), amplitude (SRS and soft LRS vs. LRS), and tempo (slow SRS vs. fast SRS). Males responded more strongly to SRS than to LRS or soft LRS, indicating that song structure had a greater effect on response than song amplitude. SRS tempo did not detectably affect male response. Importantly, males responded more strongly to SRS when their mates were fertile, presumably because hearing SRS can indicate that a male’s mate is being courted by an intruding male and a strong response can deter extrapair competitors. We conclude that low-amplitude songs can function in both inter- and intrasexual communication and should receive greater attention in future studies of mate choice and male-male competition.
De novo transcriptome sequencing in a songbird, the dark-eyed junco (Junco hyemalis): Genomic tools for an ecological model system
(BMC Genomics, 2012-07-09) Peterson, Mark P.; Whittaker, Danielle J.; Ambreth, Shruthi; Sureschandra, Suhas; Buechlein, Aaron; Podicheti, Ram; Choi, Jeong-Hyeon; Lai, Zhao; Mockatis, Keithanne; Colbourne, John; Tang, Haixu; Ketterson, Ellen D.
Though genomic-level data are becoming widely available, many of the metazoan species sequenced are laboratory systems whose natural history is not well documented. In contrast, the wide array of species with very well-characterized natural history have, until recently, lacked genomics tools. It is now possible to address significant evolutionary genomics questions by applying high-throughput sequencing to discover the majority of genes for ecologically tractable species, and by subsequently developing microarray platforms from which to investigate gene regulatory networks that function in natural systems. We used GS-FLX Titanium Sequencing (Roche/454-Sequencing) of two normalized libraries of pooled RNA samples to characterize a transcriptome of the dark-eyed junco (Junco hyemalis), a North American sparrow that is a classically studied species in the fields of photoperiodism, speciation, and hormone-mediated behavior.
Testosterone Affects Neural Gene Expression Differently in Male and Female Juncos: A Role for Hormones in Mediating Sexual Dimorphism and Conflict
(PLOS One, 2013-04-16) Peterson, Mark P.; Rosvall, Kimberly A.; Choi, Jeong-Hyeon; Ziegenfus, Charles; Tang, Haixu; Colbourne, John K.; Ketterson, Ellen D.
Despite sharing much of their genomes, males and females are often highly dimorphic, reflecting at least in part the resolution of sexual conflict in response to sexually antagonistic selection. Sexual dimorphism arises owing to sex differences in gene expression, and steroid hormones are often invoked as a proximate cause of sexual dimorphism. Experimental elevation of androgens can modify behavior, physiology, and gene expression, but knowledge of the role of hormones remains incomplete, including how the sexes differ in gene expression in response to hormones. We addressed these questions in a bird species with a long history of behavioral endocrinological and ecological study, the dark-eyed junco (Junco hyemalis), using a custom microarray. Focusing on two brain regions involved in sexually dimorphic behavior and regulation of hormone secretion, we identified 651 genes that differed in expression by sex in medial amygdala and 611 in hypothalamus. Additionally, we treated individuals of each sex with testosterone implants and identified many genes that may be related to previously identified phenotypic effects of testosterone treatment. Some of these genes relate to previously identified effects of testosterone-treatment and suggest that the multiple effects of testosterone may be mediated by modifying the expression of a small number of genes. Notably, testosterone-treatment tended to alter expression of different genes in each sex: only 4 of the 527 genes identified as significant in one sex or the other were significantly differentially expressed in both sexes. Hormonally regulated gene expression is a key mechanism underlying sexual dimorphism, and our study identifies specific genes that may mediate some of these processes.

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