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Oeneis Macounii) Canadian Journal of Zoology Population genetic structure and assessment of allochronic divergence in the Macoun’s arctic butterfly (Oeneis macounii) Journal: Canadian Journal of Zoology Manuscript ID cjz-2018-0117.R1 Manuscript Type: Article Date Submitted by the 19-Jul-2018 Author: Complete List of Authors: Gradish, Angela; University of Guelph, School of Environmental Sciences Keyghobadi, Nusha; University of Western Ontario Sperling, Felix;Draft CW405a Biological Science Centre Otis, Gard; University of Guelph, School of Environmental Sciences Is your manuscript invited for consideration in a Special Not applicable (regular submission) Issue?: Macoun’s arctic butterfly, Oeneis macounii, AFLP, allochronic, Keyword: biennialism, COI, population structure https://mc06.manuscriptcentral.com/cjz-pubs Page 1 of 47 Canadian Journal of Zoology Population genetic structure and assessment of allochronic divergence in the Macoun’s arctic butterfly (Oeneis macounii) A.E. Gradish1, N. Keyghobadi2, F.A.H. Sperling3, and G.W. Otis1 1School of Environmental Sciences University of Guelph Guelph, ON, Canada N1G 2W1 [email protected]; [email protected] 2Department of Biology Western University London, ON, Canada N6A 3K7 [email protected] 3Department of Biological Sciences University of Alberta Edmonton, AB, Canada T6G 2R3 Draft [email protected] Corresponding Author: A.E. Gradish, School of Environmental Sciences, University of Guelph, Guelph, ON, Canada, N1G 2W1, 1-519-824-4120 ext. 53066, [email protected] Running Title: Population genetic structure of Macoun’s Arctic butterfly https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 2 of 47 ABSTRACT Population genetic structure and assessment of allochronic divergence in the Macoun’s arctic butterfly (Oeneis macounii) A.E. Gradish, N. Keyghobadi, F.A. H. Sperling, and G.W. Otis Patterns in the genetic variation of species can be used to infer their specific demographic and evolutionary history and provide insight into the general mechanisms underlying population divergence and speciation. The Macoun’s arctic butterfly (MA; Oeneis macounii [W. H. Edwards, 1885]) occurs across Canada and parts of the northern US in association with jack (Pinus banksiana Lamb.) and lodgepole (Pinus contorta Doug. ex Loud.) pine. MA’s current distribution is highly fragmented, and theDraft extent of reproductive isolation among allopatric populations is unknown. Furthermore, although MA is biennial, adults emerge every year in some populations. These populations presumably consist of two alternate-year cohorts, providing the opportunity for sympatric divergence via allochronic isolation. Using mitochondrial (mt) DNA and amplified fragment length polymorphism (AFLP) markers, we analyzed MA’s genetic structure to determine the current and historical role of allopatric and allochronic isolation in MA population divergence. Both markers revealed high diversity and a low, but significant, degree of spatial structure and pattern of isolation by distance. Phylogeographic structure was generally absent, with low divergence among mtDNA haplotypes. MA likely exhibits low dispersal and gene flow among most allopatric populations; however, there was no evidence of differentiation resulting from allochronic isolation for sympatric cohorts. Keywords: Macoun’s arctic butterfly, Oeneis macounii, AFLP, allochronic, biennialism, COI, population structure https://mc06.manuscriptcentral.com/cjz-pubs Page 3 of 47 Canadian Journal of Zoology INTRODUCTION Patterns of genetic variation within species are a consequence of both historical events and contemporary gene flow. At the last glacial maximum (LGM) in North America (15 – 20 ka), Canada and the northern US were covered by the Laurentide and Cordilleran ice sheets (Pielou 1991). Most species that currently inhabit these regions survived the LGM in ice-free refugia, sometimes in multiple isolated areas, and following the retreat of the ice sheets at the end of the Pleistocene, expanded their ranges into previously glaciated areas (Pielou 1991; Hewitt 1996). The genetic characteristics and geographic distributions of such species retain the signature of these past events, and therefore, they often can be used to infer their demographic and evolutionary histories, providing cluesDraft to the location of glacial refugia, post-glacial colonization routes, and vicariance events for a geographic region (Nichols and Hewitt 1994; Hewitt 1996; Avise 2000; Habel et al. 2010). For instance, if historical influences are the primary determinant of population structure, then a pattern of strong geographic genetic structuring, with high divergence among populations and unique haplotypes/alleles confined to specific geographic areas, suggests isolation in multiple refugia, their locations often corresponding to extant areas of high genetic diversity (Burg et al. 2006; Pugarin-R and Burg 2012). In contrast, a lack of geographic structuring and low divergence among populations typically corresponds to rapid post-glacial expansion from a single refugium (Pugarin-R and Burg 2012). Gene flow among populations of a species is a fundamental, on-going determinant of genetic differentiation: in its absence, populations generally diverge via genetic drift and/or adaptation to local selective factors (Slatkin 1987). Levels of gene flow may be influenced not only by geographic factors (e.g., habitat fragmentation, topographical features), but also biological characteristics of species themselves, including dispersal behaviour (Habel and https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 4 of 47 Schmitt 2009; Yamamoto and Sota 2012), phenology (Cooley et al. 2003; Santos et al. 2010; Yamamoto and Sota 2012) and host plant specificity (Peterson and Denno 1998). Thus, characterizing the genetic structure of a species can provide insight not only into its demographic history, but also the life history and behavioural traits that continue to foster its evolution (Hewitt 2001; Knowles and Carstens 2007; Schmitt et al. 2010). Our study focused on the Macoun’s arctic butterfly [MA; Oeneis macounii (W. H. Edwards)], a boreal forest species broadly distributed across much of Canada and parts of the northern United States (Layberry et al. 2001, Fig. 1). MA typically occurs in close association with mature stands of jack pine (Pinus banksiana Lamb.) or lodgepole pine (Pinus contorta Dougl. ex Loud.) (Masters 1972; Layberry et al. 2001) containing rough-leaved rice grass (Oryzopsis asperifolia Michx.), the suspectedDraft host plant of MA larvae. Currently, both pine species are fragmented, both naturally and by human activities, and consequently, although widespread, MA exists as numerous allopatric populations separated by a variety of geographic distances. The extent of reproductive isolation among such fragmented populations ultimately depends on dispersal behaviour (i.e., ability or propensity to disperse among habitat patches and the distance over which dispersal will occur) (Darvill et al. 2010). Field studies of MA are scarce, but recent observations suggest that adults display limited dispersal activity (Burns 2013), similar to some other butterfly habitat specialists (e.g., Hill et al. 1996; Schtickzelle et al. 2006). Thus, MA may exhibit significant spatial population structuring, although the geographic scale over which gene flow might be restricted is unclear. Superimposed on MA’s fragmented distribution is an asynchronous adult emergence schedule (Fig. 1). MA is biennial, requiring 2 years to complete development, with adults emerging in even- or odd-numbered years in different areas. Some literature states that MA https://mc06.manuscriptcentral.com/cjz-pubs Page 5 of 47 Canadian Journal of Zoology consists of two main, asynchronous cohorts: an even-year eastern cohort occurring from eastern Manitoba to eastern Ontario and a western cohort emerging mainly in odd years extending from western Manitoba to central British Columbia (Masters 1974; Layberry et al. 2001). However, the true pattern is more complex. In the foothills of the Rocky Mountains in Alberta and the interior of British Columbia, MA populations emerge in both years but may fly in greater numbers in either even or odd years in different areas (Sperling 1993; Bird et al. 1995; Guppy and Shepard 2001). Such seemingly annual populations in otherwise biennial animals presumably consist of two asynchronous (i.e., one emerging in even-numbered years, the other in odd-numbered years), biennial cohorts (Heliövaara et al. 1994; Brykov et al. 1996; Kankare et al. 2002). While it is feasible that extreme climatic conditions could routinely cause some individuals to emerge off-year (c.f., PowellDraft 2001), creating the opportunity for gene flow between cohorts, field observations and collection records of MA (G. W. Otis, unpublished data) suggest that this occurs very rarely: of a few thousand records, the only known off-year adults were collected in one site in SE Manitoba in 1979. Thus, these alternate-year cohorts may be reproductively isolated, creating the opportunity for sympatric, allochronic divergence. Although studies indicate that allochrony acts as an important reproductive isolating mechanism for some periodical animals (Brykov et al. 1996; Simon et al. 2000; Cooley et al. 2001; Taylor and Friesen 2017), to date the differentiation between sympatric, allochronic cohorts has only been assessed for three biennial insect species (Heliövaara et al. 1988; Väisänen and Heliövaara 1990;
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