ACCEPTED VERSION "This is the peer reviewed version of the following article: J. M. Serb, E. Sherratt, A. Alejandrino & D. C. Adams Phylogenetic convergence and multiple shell shape optima for gliding scallops (Bivalvia: Pectinidae) Journal of Evolutionary Biology, 2017; 30(9):1736-1747 © 2017 European Society for Evolutionary Biology which has been published in final form at https://doi.org/10.1111/jeb.13137 This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving." 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Authors may transmit, print and share copies of the accepted version with colleagues, provided that there is no systematic distribution, e.g. a posting on a listserve, network or automated delivery. There is no obligation upon authors to remove preprints posted to not for profit preprint servers prior to submission. 5 September 2018 http://hdl.handle.net/2440/114114 Journal of Evolutionary Biology Phylogenetic convergen ce and multiple shell shape optima for gliding scallops (Bivalvia: Pectinidae) Journal: Journal of Evolutionary Biology Manuscript ID JEB-2017-00260 Manuscript Type: Research Papers Keywords: Morphometrics, macroevolution, Mollusca, Morphology, Phylogenetics Page 11 of 57 Journal of Evolutionary Biology 1 Abstract 2 3 An important question in evolutionary biology is how often, and to what extent, 4 similar ecologies elicit the same phenotypic response in distantly related taxa. In some 5 scenarios, the repeated evolution of particular phenotypes may be expected, for 6 instance when species are exposed to common selective forces that result from strong 7 functional demands. In bivalved scallops (Pectinidae), some species exhibit a distinct 8 swimming behavior (gliding), which requires specific biomechanical attributes to 9 generate lift and reduce drag during locomotive events. Further, a phylogenetic 10 analysis revealed that gliding behavior has independently evolved at least four times, 11 which raises the question as to whether these independent lineages have also 12 converged on a similar phenotype. In this study, we test the hypothesis that gliding 13 scallops display shell shape convergence using a combination of geometric 14 morphometrics and phylogenetic comparative methods that evaluate patterns of 15 multivariate trait evolution. Our findings reveal that the gliding species display less 16 morphological disparity and significant evolutionary convergence in morphospace, 17 relative to expectations under a neutral model of Brownian motion for evolutionary 18 phenotypic change. Intriguingly, the phylomorphospace patterns indicate that gliding 19 lineages follow similar evolutionary trajectories to not one, but two regions of 20 morphological space, and subsequent analyses identified significant differences in 21 their biomechanical parameters, suggesting that these two groups of scallops 22 accomplish gliding in different ways. Thus, while there is a clear gliding morphotype 23 that has evolved convergently across the phylogeny, functionally distinct 24 morphological sub-forms are apparent, suggesting that there may be two optima for 25 the gliding phenotype in the Pectinidae. 26 Journal of Evolutionary Biology Page 12 of 57 27 Introduction 28 How often, and to what extent, do similar ecologies elicit the same phenotypic response 29 in distantly related taxa? Alike phenotypes can arise when species exploit a common trophic 30 niche and evolutionarily respond in a congruent manner to those selective constraints required 31 for particular function or biomechanical task (Herrel et al. , 2008; Vincent et al. , 2009; Adams & 32 Nistri, 2010). This is the pattern of convergence, the repeated evolution of similar traits among 33 multiple lineages that ancestrally lack the trait (Stayton, 2015), and convergent evolution is 34 regularly treated as evidence for adaptation (Harvey & Pagel, 1991; Larson & Losos, 1996). 35 Some of the best known examples of convergent evolution are seen in the similarity in body 36 plans of the succulent plants in Euphorbiaceae and Cactaceae (Alvarado-Cárdenas et al. , 2013) 37 and Old and New World anteaters (Beck et al. , 2006), or the similarity of skull shape between 38 the marsupial Thylacine (Tasmanian wolf) and that of the placental canids (Wroe & Milne, 2007; 39 Goswami et al. , 2011). 40 However, convergence need not create perfect morphological replicas. Rather, there can 41 be varying degrees of morphological variance among phenotypes even if they experience 42 selective regimes that impose similar or identical functional demands. For example, lineages may 43 converge towards a general area of morphospace, but occupy different regions within it (Herrel 44 et al ., 2004; Leal et al ., 2002; Stayton, 2006). Likewise, independent lineages may evolve to a 45 distinct region in morphospace, but the size of this region may be larger than what the 46 morphospace is for the ancestral phenotypes of those lineages (Collar et al ., 2014). Furthermore, 47 when multiple levels of biological organization are compared, one may observe convergence in 48 the ability to perform a particular task across a set of taxa, even when such taxa exhibit distinct 49 or even divergent morphologies (reviewed in Wainwright, 2007). This disconnect across the 50 functional-morphological boundary can occur when modular morphological components are Page 13 of 57 Journal of Evolutionary Biology 51 present, allowing for distinct combinations of morphological forms to create similar functional 52 properties (‘many-to-one mapping’ of form to function: Alfaro et al ., 2004; Wainwright et al ., 53 2005). 54 For evolutionary biologists, quantifying convergent patterns has long been an analytical 55 challenge, and numerous approaches have been suggested to characterize particular attributes 56 that inform on patterns and processes of convergence (Stayton, 2006, 2008; Muschick et al. , 57 2012; Arbuckle et al. , 2014). However, several recently-developed synthetic quantitative 58 measures have been proposed which characterize the overall extent to which two or more 59 lineages display convergent morphological patterns (Stayton, 2015). Importantly, these 60 approaches are process-neutral; describing only patterns of convergence, and leveraging the 61 shared phylogenetic history of the taxa under investigation when making evolutionary inferences 62 of those patterns (see Stayton, 2015). As such, these tools provide a powerful means of 63 evaluating evolutionary convergence, and provide key evidence in determining the extent to 64 which independent lineages converge on a common phenotype or display a suite of closely 65 related solutions to similar ecological challenges. 66 One the strongest illustrations for how functional demands influence morphology is the 67 many instances of convergent shell form of bivalved molluscs (Bivalvia). It has long been 68 recognized that there is a strong association between shell form and ecological niche in bivalves 69 (Verrill, 1897; Kauffman, 1969; Stanley, 1970, 1972). Stanley (1970) was the first to described 70 in detail how particular shell traits are found in species belonging to one of seven “life habit” 71 classes (sensu Stanley, 1970), which are defined by the animal’s life position relative to the 72 substrate, type of locomotion or attachment, and feeding mode (hereafter referred to as 73 “ecomorphs” sensu Williams, 1972). Thus, shell form is the evolutionary response to the external Journal of Evolutionary Biology Page 14 of 57 74 requirements for living space, locomotion, defense, and survival of the adult animal. 75 Modifications to shell morphology include changes to the overall outline of each valve (left vs. 76 right), the form along the hinge, the degree of shell inflatedness (convexity vs. concavity), or the 77 extent of ornamentation over each valve. In ecological classes with more specific performance 78 needs,