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Choristoneura Fumiferana) Group on an Isolated Forest Island Lisa M

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Choristoneura Fumiferana) Group on an Isolated Forest Island Lisa M Life-history traits maintain the genomic integrity of sympatric species of the spruce budworm (Choristoneura fumiferana) group on an isolated forest island Lisa M. Lumley & Felix A. H. Sperling Department of Biological Sciences, CW 405 Biological Sciences Centre, University of Alberta, Edmonton, AB T6G 2E9, Canada Keywords Abstract Cypress Hills, Choristoneura lambertiana, Choristoneura occidentalis, hybridization, Identification of widespread species collected from islands can be challenging due to integrative taxonomy, phenology, the potential for local ecological and phenotypic divergence in isolated populations. pheromones, speciation, species delimitation. We sought to determine how many species of the spruce budworm (Choristoneura fumiferana) complex reside in Cypress Hills, an isolated remnant coniferous forest Correspondence in western Canada. We integrated data on behavior, ecology, morphology, mito- Lisa M. Lumley, Laurentian Forestry Centre, chondrial DNA, and simple sequence repeats, comparing Cypress Hills populations Canadian Forest Service, Natural Resources Canada, 1055 du P.E.P.S., P.O. Box 10380, Stn. to those from other regions of North America to determine which species they Ste. Foy, Quebec, QC G1V 4C7, Canada. resembled most. We identified C. fumiferana, C. occidentalis, C. lambertiana,and Tel: +01 (418) 648-7149; hybrid forms in Cypress Hills. Adult flight phenology and pheromone attraction Fax: +01 (418) 648-5849; were identified as key life-history traits involved in maintaining the genomic in- E-mail: [email protected] tegrity of species. Our study highlights the importance of extensive sampling of both specimens and a variety of characters for understanding species boundaries in Received: 12 May 2011; Revised: 27 June biodiversity research. 2011; Accepted: 28 June 2011. doi: 10.1002/ece3.11 Eastwood, 2006). An increased propensity to hybridize and Introduction exchange genes may also be exhibited between closely related Islands have long fascinated biogeographers, ecologists, and species in new contact on an island (e.g., Clarke et al. 1996; evolutionary biologists, as they provide insights into the Grant et al. 1996). Our study focused on a continental is- mechanisms that shape biological diversity (MacArthur and land, Cypress Hills, where these challenges have complicated Wilson 1967; Brown and Lomolino 2000; Gillespie and Rod- the identification of conifer-feeding species present in the erick 2002; Lomolino and Brown 2009). Island biogeogra- spruce budworm (Choristoneura fumiferana Clemens 1865) phy theory encompasses the biota of oceanic islands, isolated complex (Lepidoptera: Tortricidae). continental habitats, such as lakes or mountaintops (Hughes Cypress Hills is located on the border of southern Alberta and Eastwood 2006; Thornton 2007), and habitats that have and Saskatchewan in Canada, and is a forested continental been fragmented through human activity (Harris 1984; Haila island isolated from the nearest coniferous region by ap- 2002; Thornton, 2007). However, this framework focuses on proximately 250 km (Chilton 2003). Coniferous tree species the number of species on an island as an equilibrium be- include pine (Pinus contorta DouglasexLouden)andspruce tween colonization and extinction of species, implying little (Picea glauca [Moench] Voss and P. albertiana S. Brown change in the species themselves, and is largely mute on the emend. Strong and Hills). Picea albertiana are hybrid forms subject of species identification and delimitation on islands. of P. glauca (Moench) Voss and P. engelmannii Parry ex En- Nonetheless, processes of divergence, hybridization, or spe- gelmann (Strong and Hills 2006). Based on pollen records, ciation may occur on an island, particularly since adaptive Cypress Hills is a refugium that, due to its higher elevation traits may be under increased selection pressure to adapt and higher rainfall, has allowed Picea and Pinus species to to a new environment (e.g., Grant et al. 1996; Hughes and survive, while surrounding regions developed into grassland c 2011 The Authors. Published by Blackwell Publishing Ltd. This is an open access article under the terms of the Creative 119 Commons Attribution Non Commercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. Spruce Budworm Species Delimitation L. M. Lumley & F. A. H. Sperling somewhere between 12,000 and 14,000 years before present are also known to migrate long distances, having been ob- (Strong and Hills 2005). served to disperse as far as 600 km (Dobesberger et al. 1983), The presence of these coniferous trees has allowed the col- which would allow more recent dispersal events from either onization of insect species from the spruce budworm species the boreal or cordilleran regions to populate Cypress Hills. group, a coniferophagous pest complex that ranges across The hybrid origin of one of the spruce species in Cypress the Nearctic region. This is an extremely well-studied species Hills, P. albertiana, points toward the possibility that resident group of moths that includes C. fumiferana, which is the most spruce budworm populations in Cypress Hills may also be destructive insect defoliator in North America (Volney and hybrids, formed through secondary contact of “mainland” Fleming 2007) and has become a model organism for study- boreal and cordilleran species; all species within the spruce ing insect outbreak dynamics (e.g., Greenbank et al. 1980; budworm complex have been shown to hybridize and pro- Williams and Liebhold 2000; Royama et al. 2005; Regni´ ere` duce fertile offspring in laboratory studies (Harvey 1997). and Nealis 2007). Species within the complex are not all of With Cypress Hills containing only three conifer species there equal economic importance, as some are less likely to enter is also the possibility of increased rates of selection, leading an outbreak phase and cause widespread damage. The species to speciation, for species that have immigrated from other also differ in their morphology, behavior, and bioregion as- regions but do not originally prefer spruce (P. albertiana or P. sociation. However, species identification is a challenge since glauca) or lodgepole pine. Colonizing or refugial species may these differences are frequency related rather than discrete also have to adapt to different environmental conditions in for each species (Harvey 1985; Dang 1992; Harvey 1997), Cypress Hills compared to typical conditions in their normal and multiple characters are typically necessary for species range, again possibly leading to increased rates of selection identification. Although phenotypic traits work well for iden- and speciation. tification when spruce budworm species are found in their With these considerations in mind, our objectives were to typical habitats, identifying species outside of their known determine the identity of the spruce budworm species resid- range and in locations with nontypical environmental char- ing in Cypress Hills and to determine what characteristics acteristics, such as Cypress Hills, can be very difficult. This may allow them to maintain their genomic integrity if there is further complicated by the documented ability of spruce are multiple species. Putatively neutral markers (SSRs and budworm species to hybridize and produce viable offspring mtDNA) were analyzed to measure gene flow and to deter- (Harvey 1997). Genetic markers such as mitochondrial DNA mine whether there were any hybridization events among (mtDNA) and simple sequence repeats (SSRs, also referred to species or populations within Cypress Hills, as well as to as microsatellites) can help to identify some species, but the assign individuals to previously delimited species by com- majority of the species can not be identified on the basis of paring them to “mainland” species. Adaptive traits (larval these genetic markers alone as genetic clustering is less specific host plant, pheromone attraction, adult flight phenology, and than the species boundaries. Therefore, putatively adaptive adult forewing morphometrics) were surveyed to determine phenotypic traits such as life-history traits and morphology if there were any evolutionarily significant characters that are still necessary to identify most of the species, requiring may allow species to maintain their genomic integrity while an integrative approach using multiple markers (Lumley and existing in sympatry, as well as to assist in assigning Cypress Sperling 2011). Hills individuals to species by comparing their traits with The Cypress Hills habitat island is located between two ma- those found in mainland species. Our work is intended to jor ecosystem regions hosting different species of the spruce contribute to our understanding of spruce budworm species budworm species complex (consult Lumley and Sperling interactions as well as to explore appropriate methods for 2011 for a species range map). About 400 km to the north and delimiting and identifying species on islands. east is the boreal region with C. fumiferana and C. pinus Free- man 1953. To the west is a mountainous region with the re- Materials and Methods maining six species within the complex: C. biennis (Freeman 1967), C. carnana (Barnes and Busck 1920), C. lambertiana Collections for Cypress Hills (Busck 1915), C. occidentalis (Freeman 1967), C. orae (Free- As indicated in Fig. 1 and Table S1, collected specimens that man 1967), and C. retiniana (Walsingham 1879). Described
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