Genetic Evidence for Landscape Effects on Dispersal in the Army Ant Eciton Burchellii
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Molecular Ecology (2014) 23, 96–109 doi: 10.1111/mec.12573 Genetic evidence for landscape effects on dispersal in the army ant Eciton burchellii THOMAS W. SOARE,* ANJALI KUMAR,*† KERRY A. NAISH‡ and SEAN O’DONNELL*§ *Animal Behavior Program, Department of Psychology, University of Washington, Seattle, WA 98195, USA, †Massachusetts Institute of Technology, Cambridge, MA 02139, USA, ‡School of Aquatic and Fishery Sciences, University of Washington, Seattle, WA 98195, USA, §Department of Biology, Drexel University, Philadelphia, PA 19104, USA Abstract Inhibited dispersal, leading to reduced gene flow, threatens populations with inbreed- ing depression and local extinction. Fragmentation may be especially detrimental to social insects because inhibited gene flow has important consequences for cooperation and competition within and among colonies. Army ants have winged males and per- manently wingless queens; these traits imply male-biased dispersal. However, army ant colonies are obligately nomadic and have the potential to traverse landscapes. Eciton burchellii, the most regularly nomadic army ant, is a forest interior species: col- ony raiding activities are limited in the absence of forest cover. To examine whether nomadism and landscape (forest clearing and elevation) affect population genetic structure in a montane E. burchellii population, we reconstructed queen and male genotypes from 25 colonies at seven polymorphic microsatellite loci. Pairwise genetic distances among individuals were compared to pairwise geographical and resistance distances using regressions with permutations, partial Mantel tests and random forests analyses. Although there was no significant spatial genetic structure in queens or males in montane forest, dispersal may be male-biased. We found significant isolation by landscape resistance for queens based on land cover (forest clearing), but not on elevation. Summed colony emigrations over the lifetime of the queen may contribute to gene flow in this species and forest clearing impedes these movements and subse- quent gene dispersal. Further forest cover removal may increasingly inhibit Eciton bur- chellii colony dispersal. We recommend maintaining habitat connectivity in tropical forests to promote population persistence for this keystone species. Keywords: deforestation, habitat fragmentation, isolation by distance, landscape genetics, sex-biased dispersal Received 21 November 2012; revision received 30 September 2013; accepted 15 October 2013 fragmentation can inhibit gene flow by isolating popu- Introduction lations, create inbreeding depression within subpopula- Dispersal has profound evolutionary consequences for tions, result in local extinction (Saccheri et al. 1998; many levels of biological organization (Broquet & Petit Segelbacher et al. 2010) and change species biology 2009). In continuous populations, the interaction (Fischer & Lindenmayer 2007). In tropical forest ecosys- between dispersal and genetic drift may lead to isola- tems, habitat fragmentation has altered species richness, tion by distance (Slatkin & Maddison 1990; Hardy & abundances and interactions, and affected ecosystem Vekemans 1999) and the balance between dispersal and processes such as nutrient cycling (Bierregaard et al. selection can influence adaptive evolution and specia- 1992; Laurance et al. 2002). tion (Turelli et al. 2001). Dispersal restricted by habitat Fragmentation may have significant effects on Hyme- noptera, which are haplodiploid and generally have a Correspondence: Thomas W. Soare, Fax: +1 206 685 3157; lower effective population size and less molecular vari- E-mail: [email protected] ation than diploids (Hedrick & Parker 1997). Gene flow © 2013 John Wiley & Sons Ltd LANDSCAPE AFFECTS DISPERSAL IN ARMY ANTS 97 in social insects may have important consequences for colonies at high elevations are probably living at the cooperation and competition within colonies, among lower limit of their thermal tolerance (O’Donnell & colonies and among populations (Pamilo et al. 1997; Kumar 2006; O’Donnell et al. 2011; Soare et al. 2011), Ross 2001). Evolutionary processes are of particular high elevations may inhibit dispersal uniformly. Alter- interest in nomadic army ants (Eciton burchellii) because natively, colonies may be locally adapted to and may they are top predators and ecological keystones in Neo- preferentially disperse within their natal elevation band; tropical forests (Franks 1982; Franks & Bossert 1983; elevation bands are coarsely correlated with Holdridge Kaspari et al. 2011). life zones (Holdridge 1967; Haber 2000). In undisturbed ant populations, dispersal is primarily The specific aim of this study was to determine determined by the mode of colony founding: indepen- whether landscape variables (forest fragmentation and dent founding by flying queens or dependent founding elevation) affect recent gene flow in army ants. To where queens are accompanied by flightless workers achieve this aim, we determined whether colony emi- (Pamilo et al. 1997; Peeters & Ito 2001; Ross 2001). Dis- grations contributed to gene dispersion by comparing persal of dependent foundresses is determined by the spatial genetic structure (SGS) across castes (workers, distance over which they can walk and therefore is queens and males) sampled after dispersal. We then more limited than that of independent foundresses compared relatedness patterns among queens with (Pamilo et al. 1997; Peeters & Ito 2001; Sundstrom€ et al. competing isolation by landscape resistance models to 2005). Male ants are winged in most species (Holldobler€ examine the effects of forest clearing and elevation on & Wilson 1990); therefore, male-biased dispersal is more colony dispersal. We used a landscape genetics strongly associated with dependent colony founding in approach and sampled at the level of individuals with- ants (Pamilo et al. 1997; Sundstrom€ et al. 2005). out identifying populations in advance, enabling detec- Regular colony emigrations have the potential to con- tion of SGS (e.g. isolation-by-distance patterns: Rousset tribute to gene flow in nomadic army ants. Eciton burch- 2000; Hazlitt et al. 2004; Hardy et al. 2008; Banks & ellii army ant colonies are monogynous and reproduce Peakall 2012; Ivens et al. 2012) and comparison of rela- by fission. Two giant wingless queens each walk away tive influence of landscape variables on contemporary with half of the worker force (Schneirla 1971; Gotwald gene flow (Manel et al. 2003; Segelbacher et al. 2010; 1995; Kronauer 2009). Virgin queens mate immediately Storfer et al. 2010; Short Bull et al. 2011). with multiple males and store this sperm for the rest of their lives (Kronauer et al. 2006; Kronauer & Boomsma Methods 2007). Because army ants reproduce by colony fission but males are winged, dispersal may be male-biased. We sampled 25 Eciton burchellii colonies in Neotropical Previous genetic studies of army ants have detected montane forest around Monteverde, Costa Rica, from 15 high rates of polyandry (Kronauer et al. 2006) and evi- Jul 2006 to 16 Sep 2006 over 4.6 km E-W and 9.3 km N- dence for male-biased dispersal (Berghoff et al. 2008; S and across 600 m of elevation. We located colonies Perez-Espona et al. 2012a). However, army ant colonies through systematic trail walks and opportunistic have a regular two week nomadic period tied to their encounters (Vidal-Riggs & Chaves-Campos 2008; five-week reproductive cycle while the larvae are grow- Kumar & O’Donnell 2009; Soare et al. 2011), thus ing (Schneirla 1971; Franks & Fletcher 1983) and cover assuming a continuously distributed population and hundreds of metres during this time (Franks & Fletcher independence of observations (Storfer et al. 2007). Addi- 1983; Willson et al. 2011). tional details regarding the study site, sample collection Landscape variables may primarily affect queen dis- and genotyping can be found in the Supporting infor- persal by restricting colony emigrations. Despite regular mation (Data S1, Tables S1, S2). obligate nomadism and a wide geographical range, the army ant Eciton burchellii is a forest interior species Genetic analysis (Schneirla 1971; Meisel 2006) and populations are vul- nerable to local extinction in forest fragments (Partridge We reconstructed queen and male genotypes from 13– et al. 1996; Boswell et al. 1998; Meisel 2004) and agroeco- 20 worker genotypes from each of 25 colonies (Table systems (Roberts et al. 2000). In lowland rainforest, Eci- S1) in the program COLONY 2.0 (Jones & Wang 2010). ton burchellii avoids entering open areas (Meisel 2006) To test the effects of genotyping error and to confirm and deforestation might inhibit dispersal (Perez-Espona reliability, we repeated COLONY analyses with error et al. 2012a). Colonies increasingly forage in open areas rates ranging from 0 to 5% and multiple random num- at high elevations (Kumar & O’Donnell 2009), and thus ber seeds. We calculated overall and within locus fragmentation in montane forest may or may not inbreeding among queen genotypes (FIq) in SPAGeDi impede gene flow. Furthermore, because Eciton burchellii 1.3 (Hardy & Vekemans 2002) and tested for linkage © 2013 John Wiley & Sons Ltd 98 T. W. SOARE ET AL. disequilibrium among all pairs of loci in queen geno- In order to further evaluate the power of our types using FSTAT 2.9.3.2 (Goudet 2002) with 420 per- approach, we compared our data to a recent landscape mutations (Bonferroni adjusted nominal P = 0.0024). genetics study of a population of Eciton burchellii foreli The effective mating frequency