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How Parallel Is Parallel Evolution? a Comparative Analysis in Fishes

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How Parallel Is Parallel Evolution? a Comparative Analysis in Fishes vol. 190, no. 1 the american naturalist july 2017 How Parallel Is Parallel Evolution? A Comparative Analysis in Fishes Krista B. Oke,1,* Gregor Rolshausen,1,2 Caroline LeBlond,1 and Andrew P. Hendry1 1. Redpath Museum and Department of Biology, McGill University, 859 Sherbrooke Street West, Montreal, Quebec H3A 2K6, Canada; 2. Senckenberg Biodiversity and Climate Research Centre (BiK-F), Senckenberganlage 25, 60325 Frankfurt am Main, Germany Submitted September 12, 2016; Accepted February 14, 2017; Electronically published April 26, 2017 Online enhancements: appendix. Dryad data: http://dx.doi.org/10.5061/dryad.bb206. abstract: Evidence of phenotypic parallelism is often used to infer Fox 2002; Langerhans and DeWitt 2004; Langerhans et al. the deterministic role played by natural selection. However, variation in 2006; Rosenblum and Harmon 2010) and within species the extent or direction of divergence is often evident among indepen- (e.g., Hoekstra and Nachman 2003; Landry and Bernatchez dent evolutionary replicates, raising the following question: just how 2010; Kaeuffer et al. 2012; Ravinet et al. 2013a; Fitzpatrick parallel, overall, is parallel evolution? We answer this question through et al. 2014; Moore et al. 2016). Many potential factors (or any a comparative analysis of studies of fishes, a taxon where parallel evolu- combination of them) could cause this extensive (non)par- fi tion has been much discussed. We rst ask how much of the among- allelism, including (1) variation in natural selection despite population variance in phenotypic traits can be explained by different “ ” seemingly parallel environments or the use of overly sim- environment types, such as high predation versus low predation or fi benthic versus limnetic. We then use phenotypic change vector analysis pli ed habitat categories (Berner et al. 2008; Kaeuffer et al. to quantify variation in the direction (vector angles) and magnitude 2012; Moore et al. 2016); (2) differences in genetic factors, (vector lengths) of environment-associated divergence. All analyses such as drift, mutation, gene flow, and past selection (Hen- show high variation in the extent of parallelism—from very high to very dry et al. 2001; Schluter et al. 2004; Bolnick and Nosil 2007); low, along with everything in between—highlighting the importance of (3) variation in sexual selection (Bonduriansky 2011; Maan quantifying parallelism rather than just asserting its presence. Interest- and Seehausen 2011); and (4) alternative phenotypic solu- ingly, instances of low extents of parallelism represent important com- ponents of divergence in many cases, promising considerable opportu- tions to the same functional problem (Gould and Lewontin nities for inferences about the factors shaping phenotypic divergence. 1979; Arnold 1983; Alfaro et al. 2004; Wainwright et al. 2005). Thus, deviations from strict phenotypic parallelism Keywords: parallel evolution, convergent evolution, nonparallel evolu- provide a useful substrate for exploring the relative impor- fi tion, repeatability, shes. tance of these different forces in shaping the diversity of life. The utility of such endeavors will depend on just how vari- Introduction able the extent of parallelism typically is in nature. Here, we consider the extent of parallelism in studies of parallel evolu- The independent evolution of similar traits in similar envi- tion by means of a comparative analysis across studies in the ronments is classically used to support a deterministic role fish literature. for natural selection in shaping evolution. At the phenotypic Our analysis focuses on fishes, which present several rele- level, this pattern has been variously called evolutionary vant benefits (see also Moore et al. 2016). First, fishes are a “repeatability,”“predictability,”“parallelism,” or “conver- highly diverse group of well-studied organisms that include gence” (Clarke 1975; Langerhans et al. 2004; Arendt and several classic examples of parallel evolution, such as high- Reznick 2008; Losos 2011; Wake et al. 2011); we will use predation versus low-predation guppies (Poecilia reticulata; the term “parallelism” owing to its predominance in the lit- e.g., Reznick and Endler 1982), benthic versus limnetic three- erature for our focal taxon. Increasingly, however, many spine stickleback (Gasterosteus aculeatus; e.g., Schluter and cases are being described of considerable variation in the ex- McPhail 1992), and sulfidic versus nonsulfidic spring live- tent of phenotypic similarity among populations from sim- bearing fish (often also comparing cave vs. surface popula- ilar environments, both between species (Brinsmead and tions; Poecilia mexicana; e.g., Tobler et al. 2011; Riesch et al. 2016). Second, fishes have a reasonably common set of phe- * Corresponding author; e-mail: [email protected]. notypic traits that facilitate among-species comparisons of Am. Nat. 2017. Vol. 190, pp. 1–16. q 2017 by The University of Chicago. within-species parallelism. Examples include body shape (e.g., 0003-0147/2017/19001-57255$15.00. All rights reserved. Taylor et al. 1997; Østbye et al. 2005; Adams et al. 2008; DOI: 10.1086/691989 Kaeuffer et al. 2012; Ingley et al. 2014a), numbers and sizes This content downloaded from 132.216.002.229 on June 21, 2017 08:51:00 AM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 2 The American Naturalist of offspring (e.g., Reznick et al. 1996; Jennions and Telford be due to variation in the direction of selection (Landry and 2002; Kavanagh et al. 2010; Riesch et al. 2013), and gill raker Bernatchez 2010; Kaeuffer et al. 2012; Fitzpatrick et al. 2014), traits (Taylor and Bentzen 1993; Palkovacs et al. 2008; Mat- whereas variation in the magnitude of divergence might be thews et al. 2010; Tobler et al. 2011; Evans et al. 2013; Theis due to variation in constraints, such as gene flow (Hendry et al. 2014a). Third, population divergence into different en- and Taylor 2004; Bolnick and Nosil 2007). Although it might vironments often occurs independently in different water- be tempting to consider variation only in direction when sheds, providing ample evolutionary replication to assess par- evaluating parallel evolution, variation in magnitude is also allelism (e.g., Johnson 2001; Østbye et al. 2006; Tobler et al. critical. Imagine a scenario where multiple ecotype pairs all 2011; Kaeuffer et al. 2012). diverge in the same direction, but half of the pairs show very Most studies of phenotypic parallelism seek only to infer slight (presumably biologically unimportant) differences and its existence, often by simply considering the significance of the other half show very large (presumably biologically im- a grouping factor, such as “environment” (the term we will portant) differences. Despite similar directions of divergence use for habitat types) or “ecotype” (the term we will use for in all pairs, invoking strong parallelism would be unhelpful population types), in statistical models analyzing multiple and misleading. Hence, quantification of parallelism should populations from multiple environments. This qualitative consider variation in both the magnitude and the direction yes-or-no approach fails to inform just how parallel the in- of divergence, separately and in combination. Hence, when ferred parallel evolution is, and it also discourages investi- discussing parallelism as a general phenomenon, we consider gations into the causes of deviations from strict parallelism. variation in both the direction and the magnitude of diver- Therefore, along with other recent investigators (e.g., Lang- gence. We use the term “(non)parallelism” to refer, in gen- erhans and DeWitt 2004; Schluter et al. 2004; Berner et al. eral, to the potential for deviations from strict parallelism 2008; Kaeuffer et al. 2012), we feel it is critically important or variability among ecotype pairs in their extent of parallel- to quantify and emphasize the extent of phenotypic par- ism. However, when referring specifically to results from the allelism. Quantification can come in several forms, which vector analyses that separate these two components, we use we here illustrate by reference to a common study design: the more explicit terms “similarity in direction” and “similar- two ecotypes (e.g., high predation vs. low predation, benthic ity in magnitude.” vs. limnetic, sulfidic vs. nonsulfidic) from each of multiple The quantitative assessment of the extent of parallelism, independent origins (typically the pairs are from separate which we undertake in the present article, not only informs watersheds). In this classic design, a researcher can ask sev- just how parallel parallel evolution is but also emphasizes eral questions, the first two focusing on trait-by-trait anal- the utility of the concept of (non)parallelism for inferring yses and the second two on multidimensional trait analyses. the ecological and evolutionary drivers of diversification. First, how often is the direction of environment-associated We investigate the extent of parallelism in published studies trait divergence (e.g., deeper bodies in benthic than limnetic of parallel evolution in fishes to ask the question, how par- fish, more offspring in high-predation than low-predation allel is parallel evolution? fish) the same across multiple evolutionary replicates? Sec- ond, how much of the variation among population trait Methods means (or among all individuals) can be explained by the en- vironment (or ecotype) term in a statistical model? Three, We
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