Abstract

The Trinidadian guppy is emblematic of parallel and convergent evolution, with repeated demonstrations that predation regime is a driver of adaptive trait evolution. A classic and foundational experiment in this system was conducted by John Endler 40 years ago, where male guppies placed into low‐predation environments in the laboratory evolved increased color in a few generations. However, Endler's experiment did not employ the now typical design for a parallel/convergent evolution study, which would employ replicates of different ancestral lineages. We therefore implemented an experiment that seeded replicate mesocosms with small founding populations of guppies originating from high‐predation populations of two very different lineages. The different mesocosms were maintained identically, and male guppy color was quantified every four months. After one year, we tested whether male color had increased, whether replicates within a lineage had parallel phenotypic trajectories, and whether the different lineages converged on a common phenotype. Results showed that male guppy color generally increased through time, primarily due to changes in melanic color, whereas the other colors showed inconsistent and highly variable trajectories. Most of the nonparallelism in phenotypic trajectories was among mesocosms containing different lineages. In addition to this mixture of parallelism and nonparallelism, convergence was not evident in that the variance in color among the mesocosms actually increased through time. We suggest that our results reflect the potential importance of high variation in female preference and stochastic processes such as drift and founder effects, both of which could be important in nature.

Highlights

  • Ecological or environmental pressures that shape natural se‐ lection can be so strong that similar phenotypes will evolve in multiple independent populations exposed to similar environ‐ ments, a phenomenon variously called “parallelism,” “conver‐ gence,” “predictability,” or “repeatability” (Arendt & Reznick, 2008; Clarke, 1975; Langerhans, Layman, Shokrollahi, & DeWitt, 36 | www.ecolevol.org Ecology and Evolution. 2019;9:36–51. | 372004; Losos, 2011; Oke, Rolshausen, LeBlond, & Hendry, 2017; Schluter, 2000; Wake, Wake, & Specht, 2011)

  • We introduced a mixture of the two lineages into each of three other mesocosms to generate insights into whether admixed populations might show qualitatively different patterns than “pure” populations, possibly due to an increase in genetic variation on which selection could act

  • A large‐scale, yearlong experiment in which replicate laboratory mesocosms were seeded with small founding populations of gup‐ pies was used to assess how a common environment shapes parallel andconvergent phenotypic changes

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Summary

Introduction

Ecological or environmental pressures that shape natural se‐ lection can be so strong that similar phenotypes will evolve in multiple independent populations exposed to similar environ‐ ments, a phenomenon variously called “parallelism,” “conver‐ gence,” “predictability,” or “repeatability” (Arendt & Reznick, 2008; Clarke, 1975; Langerhans, Layman, Shokrollahi, & DeWitt, 36 | www.ecolevol.org Ecology and Evolution. 2019;9:36–51. | 372004; Losos, 2011; Oke, Rolshausen, LeBlond, & Hendry, 2017; Schluter, 2000; Wake, Wake, & Specht, 2011). Following the geo‐ metric perspective advocated by a number of authors (Bolnick, Barrett, Oke, Rennison, & Stuart, 2018; Stuart et al, 2017), we will use the term “parallel” when referring to evolution along sim‐ ilar phenotypic trajectories and “convergence” when referring to populations with initially different phenotypes that subsequently evolve more similar phenotypes Evidence for these phenomena has been found in a wide variety of taxa ranging from viruses and bacteria (e.g., Travisano, Mongold, Bennett, & Lenski, 1995; Saxer, Doebeli, & Travisano, 2010; Wake et al, 2011) to invertebrates (e.g., Kilias, Alahiotis, & Pelecanos, 1980; Jones, Culver, & Kane, 1992), vertebrates (e.g., Losos, 1992; Langerhans et al, 2004; Romero, 2011), and plants (e.g., Wang & Qiu, 2006). We were interested in exploring the extent of nonparallelism and nonconvergence in a study system where parallelism and conver‐ gence are typically emphasized

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