Fluctuating Environments, Sexual Selection and the Evolution of Flexible Mate Choice in Birds Carlos A. Botero1*¤, Dustin R. Rubenstein2 1 National Evolutionary Synthesis Center, Durham, North Carolina, United States of America, 2 Department of Ecology, Evolution and Environmental Biology, Columbia University, New York, New York, United States of America Abstract Environmentally-induced fluctuation in the form and strength of natural selection can drive the evolution of morphology, physiology, and behavior. Here we test the idea that fluctuating climatic conditions may also influence the process of sexual selection by inducing unexpected reversals in the relative quality or sexual attractiveness of potential breeding partners. Although this phenomenon, known as ‘ecological cross-over’, has been documented in a variety of species, it remains unclear the extent to which it has driven the evolution of major interspecific differences in reproductive behavior. We show that after controlling for potentially influential life history and demographic variables, there are significant positive associations between the variability and predictability of annual climatic cycles and the prevalence of infidelity and divorce within populations of a taxonomically diverse array of socially monogamous birds. Our results are consistent with the hypothesis that environmental factors have shaped the evolution of reproductive flexibility and suggest that in the absence of severe time constraints, secondary mate choice behaviors can help prevent, correct, or minimize the negative consequences of ecological cross-overs. Our findings also illustrate how a basic evolutionary process like sexual selection is susceptible to the increasing variability and unpredictability of climatic conditions that is resulting from climate change. Citation: Botero CA, Rubenstein DR (2012) Fluctuating Environments, Sexual Selection and the Evolution of Flexible Mate Choice in Birds. PLoS ONE 7(2): e32311. doi:10.1371/journal.pone.0032311 Editor: Marty L. Leonard, Dalhousie University, Canada Received December 2, 2011; Accepted January 26, 2012; Published February 16, 2012 Copyright: 2012 Botero, Rubenstein. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: The authors acknowledge the National Evolutionary Synthesis Center (NESCent), NSF #EF-0905606, for fostering this collaboration, as well as for funding C.A.B. D.R.R was funded by Columbia University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: cabotero@ncsu.edu ¤ Current address: Initiative in Biocomplexity and Global Change Center, North Carolina State University, Raleigh, North Carolina, United States of America Introduction Local variation in precipitation and temperature (e.g., wet and dry periods, changing seasons, or El Ni n˜o events), can lead to temporal fluctuation in the form and strength of natural selection [1–5]. Such fluctuating selection (or oscillating selection, as in [1]) has been implicated in the maintenance of genetic variation under directional selection [1], and appears to be important for the evolution of morphology [1], cognition [6,7], complex social behavior [8,9], foraging flexibility [10,11], and bet-hedging [12,13]. Together, these studies suggest that fluctuating selection favors the evolution of more flexible traits by exposing individuals to a range of conditions rather than specific situations. In addition to influencing the dynamics of natural selection, it has been suggested that temporal fluctuation in environmental conditions may also play a role in the process of sexual selection [14,15]. In most sexual species, individuals attempt to maximize future direct or indirect benefits by choosing mates with superior phenotypic characteristics and/or more attractive courtship displays [16]. Because these secondary sexual characters are often plastic, sudden changes in environmental conditions can lead to unexpected reversals in the relative quality or sexual attractiveness of potential breeding options ([14,17,18] for review see [19]). Although this phenomenon, known as ecological cross-over [14], has been observed in a variety of species including mites [20], flies [21], birds [15,22], fish [23], and frogs [24], it is currently unclear the extent to which it may explain general patterns of interspecific variation in reproductive behavior. Populations exposed to frequent environmental variation may evolve flexible sexual preferences that allow individuals to select optimal partners in different ecological contexts. For example, female lark buntings, Calamospiza melanocorys, show highly variable sexual preferences among years and this variation appears to be driven by a stronger preference for the particular male trait that best predicts nesting success in any given year (e.g., beak size, wing patch size, or body color) [15]. However, when environmental change is sudden and unexpected, even species with highly flexible sexual preferences are likely to make mistakes. Furthermore, a higher prevalence of suboptimal partnerships can be expected in more variable and unpredictable habitats for at least three reasons: (1) when environmental conditions at the time of reproduction differ from those experienced during the production of sexual signals (or at the time in which females choose), courtship signals may be poor indicators of the direct benefits that a potential partner has to offer; (2) when conditions experienced by parents are likely to differ from those experienced by their offspring, current mate quality may be a poor indicator of future offspring viability (i.e., indirect benefits); and (3) when the conditions that offspring will experience are highly unpredictable, a greater genetic diversity among offspring could improve long-term PLoS ONE | www.plosone.org 1 February 2012 | Volume 7 | Issue 2 | e32311