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Habitat Structure Influences Genetic Differentiation in the Pitcher Plant Midge

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Habitat Structure Influences Genetic Differentiation in the Pitcher Plant Midge Molecular Ecology (2012) 21, 223–236 doi: 10.1111/j.1365-294X.2011.05280.x From broadscale patterns to fine-scale processes: habitat structure influences genetic differentiation in the pitcher plant midge across multiple spatial scales GORDANA RASIC and NUSHA KEYGHOBADI Department of Biology, Biological & Geological Sciences Building, University of Western Ontario, 1151 Richmond Street, London, Ontario, Canada N6A 5B7 Abstract The spatial scale at which samples are collected and analysed influences the inferences that can be drawn from landscape genetic studies. We examined genetic structure and its landscape correlates in the pitcher plant midge, Metriocnemus knabi, an inhabitant of the purple pitcher plant, Sarracenia purpurea, across several spatial scales that are naturally delimited by the midge’s habitat (leaf, plant, cluster of plants, bog and system of bogs). We analysed 11 microsatellite loci in 710 M. knabi larvae from two systems of bogs in Algonquin Provincial Park (Canada) and tested the hypotheses that variables related to habitat structure are associated with genetic differentiation in this midge. Up to 54% of variation in individual-based genetic distances at several scales was explained by broadscale landscape variables of bog size, pitcher plant density within bogs and connectivity of pitcher plant clusters. Our results indicate that oviposition behaviour of females at fine scales, as inferred from the spatial locations of full-sib larvae, and spatially limited gene flow at broad scales represent the important processes underlying observed genetic patterns in M. knabi. Broadscale landscape features (bog size and plant density) appear to influence oviposition behaviour of midges, which in turn influences the patterns of genetic differentiation observed at both fine and broad scales. Thus, we inferred linkages among genetic patterns, landscape patterns and ecological processes across spatial scales in M. knabi. Our results reinforce the value of exploring such links simultaneously across multiple spatial scales and landscapes when investigating genetic diversity within a species. Keywords: distance-based redundancy analysis, genetic structure, landscape genetics, Metri- ocnemus knabi, Sarracenia purpurea, spatial scale Received 10 December 2010; revision received 17 July 2011; accepted 20 July 2011 explored in ecological studies for more than two dec- Introduction ades (Wiens 1989; Kotliar & Wiens 1990; Holling 1992; Population genetic data are increasingly analysed Levin 1992; Wu & Loucks 1995; Wagner & Fortin 2005). within an explicitly spatial framework as more and Landscape and population genetics, however, have only more studies, largely in the growing field of landscape recently seen a strong and growing focus on spatial genetics, relate the spatial organization of genetic varia- scale questions (Anderson et al. 2010; Cushman & tion to underlying ecological processes and associated Landguth 2010; Storfer et al. 2010). landscape and environmental variables (Guillot 2009; The scale at which samples for genetic analysis are Storfer et al. 2010). Issues of scale surrounding the col- defined and collected is critical in determining the pat- lection and interpretation of spatial data have been terns observed, and the range of processes about which inferences can be made in population genetic studies Correspondence: Gordana Rasic, Fax: 519-661-3935; (Anderson et al. 2010). Both the extent and the grain of E-mail: [email protected] a study are important, where the extent represents the Ó 2011 Blackwell Publishing Ltd 224 G. RASIC and N. KEYGHOBADI total area of genetic sampling and analysis, while the The purple pitcher plant S. purpurea is found within grain represents the smallest (elementary) sampling unit acidic bogs throughout Eastern North America. It has (Anderson et al. 2010; Cushman & Landguth 2010). We developed carnivory as an adaptation to the poor nutri- cannot make reliable inferences on patterns and pro- ent environment. However, the plant’s leaves are not cesses beyond the extent of our study, nor detect any only deadly traps for different arthropods but also rep- elements of a pattern below the grain (Wiens 1989). In resent the exclusive breeding habitat for the larvae of gene flow analysis for example, study area size (extent) several insect species (Addicott 1974; Miller et al. 2002; should be larger than the area occupied by the popula- Buckley et al. 2010). For example, larvae of the pitcher tion of interest and larger than expected dispersal dis- plant midge, Metriocnemus knabi Coquillett 1904, are tances, while sampling grain should generally be usually found at the bottom of the leaf where they feed smaller than the average home-range size or dispersal on the decomposing prey of the plant. Multiple leaves distance of the study organism (Fortin & Dale 2005; are found in each plant, plants are distributed in easily Anderson et al. 2010). identifiable clusters within each bog, and bogs are eas- Population genetic patterns result from a potentially ily delineated in a landscape. These levels of habitat complex combination of evolutionary, behavioural, eco- patches (leaf, plant, cluster of plants, bog, system of logical and stochastic processes operating at different bogs) not only represent scales separated by a certain spatial and temporal scales (Balkenhol et al. 2009; spatial distance (‘distance scales’), but are also hierar- Anderson et al. 2010). Furthermore, ecological processes chically nested (‘nested scales’). Thus, the insects that and environmental variables can influence genetic vari- are commensal inhabitants (i.e. ‘inquilines’) of the pur- ation differentially at different spatial scales (Lee-Yaw ple pitcher plant represent an excellent natural system et al. 2009; Murphy et al. 2010). For example, in the bor- for ecological and genetic studies across scales. The nat- eal toad, Bufo boreas, growing season precipitation and ural features of the system remove the need for an arbi- slope temperature–moisture affect genetic connectivity trary decision on focal scales, because they offer easily of populations across multiple spatial scales, while hab- detectable habitat patches that are hierarchically nested itat permeability is only important at a fine scale (Mur- at several spatial scales. For this reason, the system has phy et al. 2010). Finally, the spatial scales of dispersal been used in landscape ecological studies to understand and other relevant processes affecting genetic variation how local interactions in the pitcher plant communities may not be known a priori, particularly in organisms (Trzcinski et al. 2005), colonization patterns (Trzcinski that are very small or display cryptic behaviours. Thus, et al. 2003), species distribution (Krawchuk & Taylor there is great value in conducting population and land- 2003) and community composition (Harvey & Miller scape genetic analyses such that multiple spatial scales 1996; Buckley et al. 2010) vary across scales. of sampling are included (Diggle & Ribeiro 2007; Sch- Our first objective in this study was to examine popu- wartz & McKelvey 2009). lation genetic structure of one of the pitcher plant’s com- Although there are many reports of genetic structure mensal inhabitants, the pitcher plant midge M. knabi, across more than one spatial scale, the majority of studies across several, nested scales. By considering samples of include only up to three scales. For example, genetic midge larvae aggregated at each scale in the spatial hier- diversity was examined at: (i) fine, population and regio- archy (leaf, plant, cluster of plants, bog, system of bogs), nal scales (riparian and mountain) in Manchurian ash we essentially changed the grain of sampling and analy- Fraxinus mandshurica (Hu et al. 2010); (ii) rivers, among sis while keeping a constant extent that is largely rela- rivers and among regions on an island in the riparian tive to the expected dispersal ability of this species plant Ainsliaea faurieana (Mitzui et al. 2010); and (iii) pop- (Krawchuk & Taylor 2003). Our second objective was to ulation, watershed and drainage scales in steelhead On- test explicit hypotheses about the effects of landscape corhynchus mykiss (Nielsen et al. 2009). While the scales of variables on genetic structure of the midge across scales. analysis in these examples reflect natural hierarchies of Specifically, results obtained under our first objective spatial organization, such as river–watershed–drainage, suggested that broader-scale landscape variables related in many other studies, the scales of analysis are appar- to habitat amount and isolation may influence spatial ently arbitrary or based primarily on an anthropocentric patterns of genetic variation observed at both fine (leaf, perception of nature. In some cases, even political bound- plant) and broad (cluster, bog) scales. As such, we used aries may be used to define scales of sampling (Blanquer distance-based redundancy analysis to explicitly test the & Uriz 2010; Gonc¸alves da Silva et al. 2010). Here, we hypothesis that bog size, plant density, or isolation of take advantage of a unique study system associated with clusters influence patterns of genetic structure at a range commensal inhabitants of the purple pitcher plant, Sarra- of scales. Although there are many potential landscape cenia purpurea L., to examine patterns of genetic variation correlates of genetic structure (e.g. Murphy et al. 2010), across multiple, objectively defined, nested spatial scales. we focused on variables related to habitat
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