Literature survey

We searched the ISI Web of Science database from 2003 to 2012 using the topic search terms “converg* evolution”, “parallel evolution”, “homoplas*”, “functional* redundan*”, and “many-to-one” refined to the categories of evolutionary biology and ecology, and excluding plant sciences. Restricting our search to the last decade and by topic area was necessary because of the volume of articles uncovered (see below). Although our survey was not exhaustive (and it may have also missed examples of repeated adaptive evolution specific to aggressive mimicry or aposematic coloration; but see Additional file 3: Table S1), it should still provide a reasonable overview of the recent literature on repeated evolution. Searches were performed between April 24 and June 13 2013. Of the 2,602 articles found, we excluded review articles, conference abstracts, opinion pieces and book chapters. The titles and abstracts of the remaining articles were examined in detail and those that were found to be relevant animal examples of repeated evolution were downloaded through the University of New South Wales library (96 papers, see Additional file 3: Table S1; NB: papers for which electronic copies could not be obtained were not included in our analyses). Two papers that we were aware of and published in 2013 were also included (i.e., [39] and [40]).

We assessed each downloaded paper to confirm that the report was of a compelling case of repeated adaptive evolution in extant taxa. Specifically, that a functionally equivalent phenotypic characteristic evolved independently in different lineages and was likely to be the product of natural or sexual selection based on an empirical study reported in the article or the citation of a previous study in which the adaptive function of the characteristic had been reputedly assessed. We restricted our survey to extant taxa because of the problems of adequately identifying examples of repeated evolution in extinct animals (see [20] for discussion). Of those articles meeting our criteria, we then compiled information on the type of phenotypic characteristic involved, the taxonomy of the animals, the likely selection pressure driving the repeated evolution, and classified whether the adaptation was an example of parallel, convergent, or functional redundant evolution based on the definitions given in Table 1. For example, adaptations classified as examples of parallel evolution were those in which some aspect of the genetic pathway underlying the characteristic had been shown to be shared among taxa. It should be noted, however, that the vast majority of studies uncovered by our literature search did not examine the genetics of repeated evolution (87 of 96 articles). Given this, there were almost certainly cases classified as convergent that may have in fact originated through parallel evolution and have yet to be determined as such (see Table 1). To help bolster our coverage of cases in which the genetics of repeated adaptive evolution had been investigated, we included 14 additional cases identified by Conte et al. ([23]; 11 of which were confirmed cases of parallel evolution). This earlier study included nine other examples that were either already included in our data set (seven) or were specific to plants (two).

In the case of functionally redundant adaptations, many authors did not distinguish such adaptations from classical convergence. We therefore classified these examples based on whether the phenotypic characteristics reported to be functionally convergent were likely to be the same or different based on character descriptions presented in papers. In some cases, similar adaptations classified as convergent may in fact be more broadly functionally redundant. For example, Caribbean Anolis ecomorphs share key morphological characteristics such as particular limb lengths depending on the size of the perches used by a species belonging to an ecomorph category (reviewed by [41]). However, changes in limb length might have occurred in a variety of ways, such as increases in the femur or tibia, or both. Unless differences in the phenotypic characteristics were clearly described in the article, we classified examples as convergent, but point out—as with the case of distinctions between parallel and convergent—that these classifications may change as additional information becomes available with future research. Finally, we also contacted two experts familiar with the phenomenon of functional redundancy who provided us with additional examples that were not uncovered during our initial literature search (NB: four of these studies were published before 2003 and we included these in an effort to increase our sample size).

We used two estimates of the phylogenetic distance separating convergent taxa. First, we obtained an estimate in millions of years, either as reported directly in the paper or from a reference cited in the paper. Where this was not found, we used the mean estimate of time since divergence from TimeTree [42] based on a search of species or genera names (see Additional file 3: Table S1). Second, we used the taxonomic separation of reported taxa. For example, the taxonomic separation of Caribbean Anolis lizards convergent in morphology [43] was ‘genus’, whereas the maximum taxonomic separation of lizards convergent in morphology from the genera Holbrookia, Sceloporus and Aspidoscelis [44] was ‘order’. Although estimates of time since divergence increased with the taxonomic separation of taxa, the relationship was noisy and non-linear (see Additional file 4: Figure S3). There were also a handful of examples for which we were unable to obtain time estimates on separation, but were able to determine taxonomic separation that allowed these examples to be included in at least some of our analyses (those reported in Additional file 1: Figure S1). We therefore used both measures of phylogenetic separation in our analyses, but focussed primarily on time since divergence given it avoided the potential subjective biases of taxonomic classification.

Meta-analysis

We counted the number of reported cases of repeated adaptive evolution in time bins of 20 MYA. Preliminary analyses showed this binning provided the best resolution of distribution patterns (NB: results were qualitatively similar using time bins of 5, 10, and 30 MYA). Counts of repeated adaptive evolution by taxonomic separation were made by converting taxonomic classifications into a score ranging from 1 (species) to 11 (kingdom; see Additional file 3: Table S1 and Additional file 4: Figure S3). Time bins or taxonomic categories in which no report of repeated evolution was found were treated as missing data rather than evidence for lack of repeated evolution among taxa at that phylogenetic separation. In some instances, several different papers reported repeated adaptive evolution in different characteristics among taxa from the same species group (e.g., Anolis lizards or stickleback fish). In these cases, the species group was used only once, either for the given type of characteristic being analysed (e.g., a behavioral characteristic in analyses of behavioral convergence – see below) or the earliest publication for that species group in analyses of broad trends (e.g., those in Fig. 2a). This ensured that highly studied groups did not skew our analyses and that the number of reports examined reflected convergence among different taxa, rather than the number of characteristics studied for the same group or the number of times the same characteristic has been studied for a species group.

To assess statistical trends in the distribution of reports of repeated adaptive evolution as a function of phylogenetic separation, we applied generalized linear models with a poisson error distribution (commonly known as a ‘count regression’) using R ver 3.0.2 (R Development Core Team). From these models, we compared the computed slope and effect size (z value) to evaluate the influence of phylogenetic distance on the probability of repeated evolution; however full model outputs are also provided in Additional file 5: Table S2. The diversity of taxa included in these analyses represented an equally diverse range of generation times. However, taxonomic groups representing short generation times (e.g., insect or fish) or long generation times (e.g., mammals) were well represented across all divergence times and taxonomic distances (fig. S1). That is, patterns of repeated adaptive evolution were unlikely to have been skewed by an over representation of certain groups with short or long generation times clustered at particular phylogenetic distances. Nevertheless, to confirm our findings were consistent, we conducted a separate set of analyses on instances of repeated evolution in fish, which were the largest taxonomic group represented in our data set (Fig. 1a) and were broadly similar in their generation times.

To further benchmark our findings, we also estimated the expected distribution of repeated adaptive evolution if its occurrence was unrelated to the phylogenetic separation of taxa (i.e., historically contingent effects on the outcome of adaptation were absent). Here, the likelihood of repeated evolution should be proportional to the number of potential species-pairs across the phylogeny. At the outset, we can make the general prediction that instances of repeated evolution should tend to be clustered among distantly related taxa rather than closely related taxa simply because there are more distantly related species pairs than closely related pairs on any phylogeny. Nevertheless, the specific distribution of potential species pairs will depend on the general properties of the phylogeny, in particular the age and frequency of rapidly radiating lineages within the tree (e.g., see [28]). Rather than use an artificially generated phylogeny, we chose two large time-calibrated phylogenies for mammals [45] and squamates (snakes and lizards; [36]). We reasoned that these would provide a more realistic and representative picture of probable patterns of repeated adaptive evolution on the tree of life than those obtained from a contrived phylogeny. We selected the phylogenies of mammals and squamates because these represented key taxonomic groups covered by our meta-analysis, included a large and diverse range of species (5,020 and 4,162 species, respectively), were time calibrated and species-level phylogenies (rather than genera or family level phylogenies), and could be readily downloaded from the supplementary information of each source.

We computed the length of time between all possible combinations of species pairs by extracting the variance-covariance matrices for each phylogeny using the R package ‘caper’ ver 0.5.2 [46]. The distribution of these distances were then plotted to provide an estimate on where instances of repeated evolution should be concentrated if the evolution of similar adaptations in different taxa were unrelated to the length of time separating taxa.