PUBLISHED VERSION Hereward, J. P.; Walter, Gimme H.; DeBarro, P. J.; Lowe, Andrew; Riginos, C. Gene flow in the green mirid, Creontiades dilutus (Hemiptera: Miridae), across arid and agricultural environments with different host plant species, Ecology and Evolution, 2013; 3(4):807-821. © 2013 The Authors. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. PERMISSIONS http://onlinelibrary.wiley.com/journal/10.1002/%28ISSN%292045- 7758/homepage/ForAuthors.html All articles accepted from 14 August 2012 are published under the terms of the Creative Commons Attribution License. All articles accepted before this date, were published under a Creative Commons Attribution Non-Commercial License. 7th August 2013 http://hdl.handle.net/2440/78979 Gene flow in the green mirid, Creontiades dilutus (Hemiptera: Miridae), across arid and agricultural environments with different host plant species J. P. Hereward1,3, G. H. Walter1, P. J. DeBarro2, A. J. Lowe4,5 & C. Riginos1 1School of Biological Sciences, The University of Queensland, Brisbane, Qld, 4072, Australia 2CSIRO Ecosystem Sciences, GPO Box 2583, Brisbane, Qld, 4001, Australia 3Cotton Catchment Communities CRC, Australian Cotton Research Institute, Locked Mail Bag 1001, Narrabri, NSW, 2390, Australia 4Australian Centre for Evolutionary Biology and Biodiversity, School of Earth and Environmental Sciences, University of Adelaide, SA, 5005, Australia 5State Herbarium of South Australia and Science Resource Centre, Department of Environment and Natural Resources, Hackney Road, SA, 5005, Australia Keywords Abstract Agriculture, dispersal, gene flow, host plant, human-altered landscapes, insect herbivore, Creontiades dilutus (Stal), the green mirid, is a polyphagous herbivorous insect microsatellite, migration, mitochondrial. endemic to Australia. Although common in the arid interior of Australia and found on several native host plants that are spatially and temporally ephemeral, Correspondence green mirids also reach pest levels on several crops in eastern Australia. These James P. Hereward, School of Biological host-associated dynamics, distributed across a large geographic area, raise ques- Sciences, The University of Queensland, tions as to whether (1) seasonal fluctuations in population size result in genetic Brisbane, Qld, 4072, Australia. Tel: +61 7 3365 2755; bottlenecks and drift, (2) arid and agricultural populations are genetically iso- E-mail: [email protected] lated, and (3) the use of different host plants results in genetic differentiation. We sequenced a mitochondrial COI fragment from individuals collected over Funding Information 24 years and screened microsatellite variation from 32 populations across two This study was possible due to PhD support seasons. The predominance of a single COI haplotype and negative Tajima D provided by the Cotton Research and in samples from 2006/2007 fit with a population expansion model. In the older Development Corporation, and the Cotton collections (1983 and 1993), a different haplotype is most prevalent, consistent CRC. with successive population contractions and expansions. Microsatellite data Received: 16 October 2012; Revised: 17 indicates recent migration between inland sites and coastal crops and admixture January 2013; Accepted: 21 January 2013 in several populations. Altogether, the data suggest that long-distance dispersal occurs between arid and agricultural regions, and this, together with fluctua- Ecology and Evolution 2013; 3(4): 807–821 tions in population size, leads to temporally dynamic patterns of genetic differ- entiation. Host-associated differentiation is evident between mirids sampled doi: 10.1002/ece3.510 from plants in the genus Cullen (Fabaceae), the primary host, and alternative host plant species growing nearby in arid regions. Our results highlight the importance of jointly assessing natural and agricultural environments in under- standing the ecology of pest insects. Introduction 2006). Insects that use native and introduced hosts thus provide a “natural experiment” to explore the likely con- Many insects that damage agricultural crops have invaded sequences of ongoing anthropogenic change in plant dis- the resources provided by agriculture across wide areas tribution and abundance. and this has generated alternative predictions as to their Few genetic studies have examined the interactions of evolutionary trajectories. Although the provision of novel insects between native host plants and agricultural resources by agriculture might promote host adaptation resources simultaneously, but the available evidence indi- (Via 1990), it has also been argued that gene flow will cates that several outcomes are possible, including increase among populations of native insects when their geographic differentiation, host-associated differentiation, range is expanded through the anthropogenic spread of and widespread gene flow. Both the rice mirid Stenotus potential hosts, making local adaptation less likely (Oliver rubrovittatus (Hemiptera: Miridae), native to Japan, and © 2013 The Authors. Ecology and Evolution published by Blackwell Publishing Ltd. This is an open access article under the terms of the Creative 807 Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Gene Flow in the Arid Adapted Green Mirid J. P. Hereward et al. Queensland fruit fly Bactrocera tryoni (Diptera: Tephriti- ference was found in genetic diversity between outbreak dae) show strong geographic differentiation (Yu et al. and non-outbreak populations (indicating that non-out- 2001; Kobayashi et al. 2011). In the former, it indicates break populations persist in sufficient size), but regional divergence across Pleistocene refuges and the latter diver- differentiation was much higher for non-outbreak popula- gence as invading crop and fruit hosts outside its original tions (Chapuis et al. 2008, 2009). Spatial and temporal var- Queensland distribution. Furthermore, an isolated fruit fly iance in population size, migration rates, and extinction population in inland Australia (Alice Springs) showed rates are predicted to not only affect mean FST, but also strong genetic evidence of a population bottleneck. Host- result in large fluctuations in the genetic differentiation associated differentiation has also been recorded in the corn between populations over time (Whitlock 1992). leafhopper Dalbulus maidis (Hemiptera: Cicadellidae), and Patterns of host-associated differentiation might be this has been associated with a shift from wild hosts to obscured by migration, bottlenecks, and population maize (Zea mays) within the last 9000 years since domesti- expansion, and interpreting the relative effects of demo- cation (Medina et al. 2012). In contrast to the above exam- graphic processes remains a challenge for empirical popu- ples, a lack of isolation by distance was found across lation genetics (Pavlidis et al. 2008; Li et al. 2012). 1700 km in the migratory moth Trichoplusia ni (Lepidop- Furthermore, host plant-associated differentiation follow- tera: Noctuidae), between its native range in California, ing host shifts is considered more likely in host specialists and crops that it seasonally invades in Canada (Franklin (Funk et al. 2002). Few studies report host-associated dif- et al. 2010). Clearly, the patterns found to date are strongly ferentiation in insects that use multiple host plants (but influenced by the biology and life history of the organism see Sword et al. 2005). Geographic differentiation gener- in question, as well as the environment it inhabits. ally appears to be higher in host plant specialists than Strong regional differentiation, as found in Stenotus ru- insects that use multiple hosts (Kelley et al. 2000; Zayed brovittatus (Kobayashi et al. 2011), and Queensland fruit et al. 2005; Gaete-Eastman et al. 2007; Habel et al. 2009; fly (Yu et al. 2001), might be expected in species that do Groot et al. 2011). This correlation is usually interpreted not regularly disperse long distances (Bohonak 1999). as a consequence of the spatial patchiness of a single Conversely, high gene flow, as documented for the migra- resource in comparison to the more widespread availabil- tory moth Trichoplusia ni (Franklin et al. 2010), has also ity of multiple resources. Resources can, however, be tem- been reported in many widespread agricultural pests porally patchy and it is not clear whether this correlation (Endersby et al. 2006, 2007; Margaritopoulos et al. 2009), would hold under these circumstances. and even in pest species thought to be relatively sedentary In this study, we examine dispersal, fluctuations in popu- (Voudouris et al. 2012). Anthropogenic and unassisted lation size, and the use of multiple host plants in Creonti- dispersal can both allow the invasion of novel resources ades dilutus, the green mirid, across its native range (and by insect populations (Stone and Sunnucks 1993; Stone host plants) in arid regions of Australia, and novel hosts et al. 2007). Such anthropogenic dispersal was thought to (agricultural crops) that it has invaded within the last be the primary mechanism allowing colonization of grain 200 years. We sampled mirids across both arid and agricul- storages by Tribolium castaneum, as this species was con- tural regions in Australia, covering most of the geographic sidered relatively sedentary