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Morphological and Genetic Concordance of Cutthroat Trout Diversification from Western North America

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Morphological and Genetic Concordance of Cutthroat Trout Diversification from Western North America Canadian Journal of Zoology Morphological and genetic concordance of cutthroat trout diversification from western North America Journal: Canadian Journal of Zoology Manuscript ID cjz-2020-0106.R2 Manuscript Type: Article Date Submitted by the 27-Nov-2020 Author: Complete List of Authors: Keeley, Ernest; Idaho State University, Department of Biological Sciences Loxterman, Janet; Idaho State University, Department of Biological Sciences Matsaw, Sammy;Draft Idaho State University, Department of Biological Sciences Njoroge, Zacharia; Idaho State University, Department of Biological Sciences Seiler, Meredith; Idaho State University, Department of Biological Sciences Seiler, Steven; Idaho State University, Department of Biological Sciences Is your manuscript invited for consideration in a Special Not applicable (regular submission) Issue?: MORPHOLOGY < Discipline, native distribution, phenotype, diversity, Keyword: intraspecific variation, cutthroat trout, Oncorhynchus clarkii © The Author(s) or their Institution(s) Page 1 of 42 Canadian Journal of Zoology 1 Morphological and genetic concordance of cutthroat trout diversification from western 2 North America 3 4 5 6 7 8 Ernest R. Keeley, Janet L. Loxterman, Sammy L. Matsaw, Zacharia M. Njoroge, Meredith B. 9 Seiler, and Steven M. Seiler 10 11 Draft 12 13 14 15 16 17 18 19 E.R. Keeley, J.L Loxterman, S.L. Matsaw, and Z. M. Njoroge. Department of Biological 20 Sciences, Stop 8007, Idaho State University, Pocatello, ID 83209, USA. 21 M.B. Seiler and S.M. Seiler. Department of Biology, Lock Haven University, Lock Haven, PA 22 17745, USA. 23 Corresponding Author: Ernest Keeley (email: [email protected]). 1 © The Author(s) or their Institution(s) Canadian Journal of Zoology Page 2 of 42 24 Abstract 25 The cutthroat trout, Oncorhynchus clarkii (Richardson, 1836), is one of the most widely 26 distributed species of freshwater fish in western North America. Occupying a diverse range of 27 habitats, they exhibit significant phenotypic variability that is often recognized by intraspecific 28 taxonomy. Recent molecular phylogenies have described phylogenetic diversification across 29 cutthroat trout populations, but no study has provided a range-wide morphological comparison of 30 taxonomic divisions. In this study, we used linear and geometric-based morphometrics to 31 determine if phylogenetic and subspecies divisions correspond to morphological variation in 32 cutthroat trout, using replicate populations from throughout the geographic range of the species. 33 Our data indicate significant morphologicalDraft divergence of intraspecific categories in some, but 34 not all, cutthroat trout subspecies. We also compare morphological distance measures with 35 distance measures of mtDNA sequence divergence. DNA sequence divergence was positively 36 correlated with morphological distance measures, indicating that morphologically more similar 37 subspecies have lower sequence divergence in comparison to morphologically distant 38 subspecies. Given these results, integrating both approaches to describing intraspecific variation 39 may be necessary for developing a comprehensive conservation plan in wide-ranging species. 40 Key words: phenotype, diversity, morphology, native distribution, intraspecific variation, 41 cutthroat trout, Oncorhynchus clarkii. 2 © The Author(s) or their Institution(s) Page 3 of 42 Canadian Journal of Zoology 42 Introduction 43 Widely distributed species often exhibit significant phenotypic variation across their 44 geographic range (Mayr 1963). Intraspecific variability can represent substantial levels of 45 diversity, allowing different populations to occupy a variety of habitats or ecological conditions 46 (Kolbe et al. 2012; Nosil 2012; Wellborn and Langerhans 2015; Des Roches et al. 2018). 47 Biologists have long recognized the importance of within-species measures of biodiversity by 48 assigning subspecies names to populations from different geographic locations that exhibit 49 phenotypic differences (Wilting et al. 2015). More recent approaches have attempted to 50 recognize within-species diversity by assigning populations to 'evolutionarily significant units' or 51 'distinct population segments' based on Draftphenotypic or genetic differences (Waples 1991; Haig 52 and D'Elia 2010). The need to use such approaches has been reinforced by examples of locally 53 adapted populations with unique morphological, behavioral, or life history characteristics (Smith 54 and Skulason 1996; Schluter 2000; Gillespie 2012; Blanquart et al. 2013). When dramatic 55 reductions in widely distributed species occur, how to implement recovery programs can be 56 complicated by a lack of understanding, or uncertainty, in identifying intraspecific diversity 57 (Bálint et al. 2011). In the face of a rapidly changing planet, maintaining the range of diversity 58 found within a species may increase the probability of species persistence and function within 59 ecosystems (Bellard et al. 2012; Des Roches et al. 2018; Raffard et al. 2019). 60 Historically, efforts to understand and describe intraspecific diversity have often occurred 61 when biologists document significant phenotypic variation among populations of a species, and 62 as a result, they describe different subspecies (Haig and D'Elia 2010; Braby et al. 2012). As 63 many subspecies names originated in the 19th and early 20th century, before the application of 64 quantitative statistical techniques, subspecies descriptions are frequently only qualitative in form 3 © The Author(s) or their Institution(s) Canadian Journal of Zoology Page 4 of 42 65 and may be based on limited geographic sampling (Remsen 2010; Winker 2010). The 66 widespread occurrence of habitat alteration and fragmentation has raised numerous concerns for 67 many taxa, often resulting in the need to reevaluate their distribution and conservation status 68 (Haig et al. 2006; Hanski 2011). The development of modern DNA technologies and molecular 69 markers has facilitated the ability of biologists to identify and establish the extent of focal taxa; 70 however, the use of such molecular data has at times created conflicting views with past 71 qualitative descriptions of intraspecific variation (Apostolidis et al. 1997; Fitzpatrick 2010; 72 Huang and Knowles 2016). While DNA divergence data may provide an enticingly 73 straightforward method of defining intraspecific groups, phylogenetic grouping based on single 74 or few genetic loci may not capture recently evolved adaptive differentiation (Zink 2004; Taylor 75 and McPhail 2008; Lamichhaney et al. 2012).Draft Multivariate morphometric techniques provide an 76 additional tool for quantifying a wide range of morphological variation that can incorporate a 77 suite of phenotypic characteristics, including measures of adaptive variation (Rohlf and Marcus 78 1993; McGuigan et al. 2003; Komiya et al. 2011). Digital imaging technology has further 79 simplified and standardized the collection of morphometric data and improved the ability of 80 researchers to increase the geographic extent of samples included in analyses (Mojekwu and 81 Anumudu 2015; Cardini 2020). Despite the improvements made in quantifying intraspecific 82 variation using molecular and morphometric methods, the two approaches have often been 83 pursued in isolation of each other and sometimes leading to arguments for one method over the 84 other (Hillis 1987; Phillimore et al. 2008; Losos et al. 2012). Given the need for evaluating the 85 status of subspecies of conservation concern (Haig et al. 2006; Venter et al. 2006; IUCN 2020), a 86 better understanding of the concordance between morphometric and molecular methods in 87 quantifying intraspecific variation is greatly needed. 4 © The Author(s) or their Institution(s) Page 5 of 42 Canadian Journal of Zoology 88 The cutthroat trout, Oncorhynchus clarkii (Richardson, 1836), is a widely-distributed 89 freshwater fish species native to western North America (Behnke 1980, 1992). Since first being 90 described by Richardson (1836), numerous common and scientific names have been used to 91 describe different species, subspecies, and populations of this polytypic group (Jordan et al. 92 1930; La Rivers 1962; Behnke 1965, 1992; Trotter 2008). Current taxonomic classifications list 93 14 subspecies of cutthroat trout, two of which are thought to be extinct (Behnke 1992; Trotter 94 2008; Trotter et al. 2018). Cutthroat trout are distributed along a north-south axis from Alaska to 95 New Mexico (Fig. 1), commonly occupying stream and lake habitats in contrasting areas ranging 96 from temperate rainforests to arid desert ecosystems (Behnke 1992; Trotter 2008). Numerous 97 populations of cutthroat trout have declined in abundance or have been extirpated as a result of 98 human-induced factors including habitatDraft loss and alteration, and by competition, predation, 99 disease, and hybridization through the introduction of non-native species (Young 1995; Trotter 100 2008). Phylogenetic analyses of DNA sequence variation of cutthroat trout have revealed 101 concordance with some subspecies categories as well as more recently recognized evolutionary 102 lineages (Wilson and Turner 2009; Houston et al. 2012; Loxterman and Keeley 2012; Brunelli et 103 al. 2013; Shiozawa et al. 2018); however, little comparative data exist for range-wide 104 morphological comparisons of subspecies categories or its concordance with molecular data (for 105 some pairwise comparisons see: Qadri 1959; Dieffenbach 1966; Bestgen et al. 2019).
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