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Conserved Community Structure and Simultaneous Divergence Events in the Fig Wasps Associated with Ficus Benjamina in Australia and China

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Conserved Community Structure and Simultaneous Divergence Events in the Fig Wasps Associated with Ficus Benjamina in Australia and China View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Harper Adams University Repository Conserved community structure and simultaneous divergence events in the fig wasps associated with Ficus benjamina in Australia and China by Darwell, C.T., Segar, S.T. and Cook, J.M. Copyright, publisher and additional information: Publishers’ version distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ DOI: https://doi.org/10.1186/s12898-018-0167-y Darwell, C.T., Segar, S.T. and Cook, J.M. 2018. Conserved community structure and simultaneous divergence events in the fig wasps associated with Ficus benjamina in Australia and China. BMC Ecology, 18(1). Darwell et al. BMC Ecol (2018) 18:13 https://doi.org/10.1186/s12898-018-0167-y BMC Ecology RESEARCH ARTICLE Open Access Conserved community structure and simultaneous divergence events in the fg wasps associated with Ficus benjamina in Australia and China Clive T. Darwell1,2 , Simon T. Segar1,3 and James M. Cook1,4* Abstract Background: Localised patterns of species diversity can be infuenced by many factors, including regional spe- cies pools, biogeographic features and interspecifc interactions. Despite recognition of these issues, we still know surprisingly little about how invertebrate biodiversity is structured across geographic scales. In particular, there have been few studies of how insect communities vary geographically while using the same plant host. We compared the composition (species, genera) and functional structure (guilds) of the chalcid wasp communities associated with the widespread fg tree, Ficus benjamina, towards the northern (Hainan province, China) and southern (Queensland, Aus- tralia) edges of its natural range. Sequence data were generated for nuclear and mtDNA markers and used to delimit species, and Bayesian divergence analyses were used to test patterns of community cohesion through evolutionary time. Results: Both communities host at least 14 fg wasp species, but no species are shared across continents. Com- munity composition is similar at the genus level, with six genera shared although some difer in species diversity between China and Australia; a further three genera occur in only China or Australia. Community functional structure remains very similar in terms of numbers of species in each ecological guild despite community composition dif- fering a little (genera) or a lot (species), depending on taxonomic level. Bayesian clustering analyses favour a single community divergence event across continents over multiple events for diferent ecological guilds. Molecular dating estimates of lineage splits between nearest inter-continental species pairs are broadly consistent with a scenario of synchronous community divergence from a shared “ancestral community”. Conclusions: Fig wasp community structure and genus-level composition are largely conserved in a wide geo- graphic comparison between China and Australia. Moreover, dating analyses suggest that the functional commu- nity structure has remained stable for long periods during historic range expansions. This suggests that ecological interactions between species may play a persistent role in shaping these communities, in contrast to fndings in some comparable temperate systems. Keywords: Barcoding, Chalcidoidea, Community composition, Biodiversity, Ficus, Galler, Parasitoid, Wasp Background maintained and distributed we must investigate the Recent decades have heralded the realisation that evolutionary histories of organisms in conjunction with to understand how species diversity is generated, regional patterns and processes [1–3]. Moreover, as diver- sity is composed of species whose evolutionary viability *Correspondence: [email protected] depends partly on species interactions, it is important to 4 Hawkesbury Institute for the Environment, Western Sydney University, investigate patterns of biodiversity in a community con- Locked Bag 1797, Penrith, NSW 2751, Australia text [4, 5]. In geographically wide-ranging communities, Full list of author information is available at the end of the article © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Darwell et al. BMC Ecol (2018) 18:13 Page 2 of 16 there may be species turnover along environmental and which are unlikely to have been so strongly afected by geographical gradients, leading to high β-diversity (the glacial refugia. degree of turnover in species composition across sites), Herbivorous insects and their parasitoid enemies even if measures of local α-diversity remains the same comprise a large proportion of terrestrial biodiversity. [6]. If ecological processes are the primary force govern- As such they are of profound ecological importance ing species’ occurrences, one would predict convergence and engage in a vast repertoire of trophic interactions in community structure at a regional scale given similar [14–17]. Nevertheless, relatively little is known about the local abiotic and biotic conditions. Alternatively, spatial diversity, distribution and biology of many such insect turnover of species may facilitate divergence in commu- groups, especially in tropical regions, and there have nity composition and structure between environmentally been few studies comparing herbivore and parasitoid and geographically distinct regions [7, 8], if species are assemblages on the same host plant between geographi- lost or gained. cal regions [18]. Many insect herbivores, and the majority While considerations of community structure often of all parasitoids, belong to the insect order Hymenop- assume that niche space is flled, geographic variation tera [19] and a number of studies have focused on the in local species diversity may indicate vacant niches in multitrophic insect communities associated with the fg- some populations [9–11]. Communities utilising the pollinator mutualism [e.g. 20–26]. same resources in geographically disparate regions may Ficus is a ubiquitous tropical and sub-tropical resource, be taxonomically (and even functionally) dissimilar comprising around 750 species that provide year-round [11], suggesting that community composition and struc- fruit resources for diverse animals. Fig-wasp commu- ture may depend more strongly on stochastic recruit- nity structure is complex, typically involving coexistence ment processes, the regional species pool, phylogenetic of fve functional groups [21] or ecological guilds. Small constraints, or intrinsic diferences in the key resources herbivorous wasp species may be pollinators (guild 1) upon which communities are founded, rather than being or non-pollinators (guild 2) with both groups galling fg driven by interspecifc interactions. fowers. Tese small galler guilds are exploited by (guild One approach to better identify underlying processes, 3) kleptoparasites/inquilines (that usurp these galls) or both within and between trophic levels, and determine parasitoids. Large wasp species, in turn, may be gallers drivers of community assembly at wide geographic scales, (guild 4) of fg wall tissue or fowers, or parasitoids (guild is to compare the divergence histories of interacting spe- 5) of large gallers. While several fg wasp communities cies [12]. Communities in which species have dispersed have been studied, there have been few comparisons of at diferent times from source populations have likely entire fg wasp communities in diferent geographic areas experienced intermittent interspecifc interactions. Such [26–28] and none using molecular tools to investigate a history reduces potential for coevolutionary dynamics diversity and divergence histories (but see [29] for work to shape community assembly and increases the oppor- focussed on particular fg wasp guilds). tunities for colonisation of certain niches by other spe- Here, we focus on the wasp community of the tropi- cies. Tis may facilitate ecological dominance for early cal fg species, Ficus benjamina (Conosycea, Moraceae), colonisers that can monopolise resources and impede which is widespread and common from India to China at species at higher trophic levels that cannot invade new the northern limits of its range, and through Southeast populations until their target resources arrive. Asia to northern regions of Australia at its southern lim- Alternatively, continuous associations among spe- its. It thus occurs in both the Oriental and Australasian cies are consistent with strong coevolutionary interac- regions. Ficus section Conosycea is thought to have origi- tions leading to more specialised life-history strategies, nated in India and radiated across Asia around 35 Mya a potential concomitant increase in diversity [13], and [30]. After this, it may have ‘rafted’ across the Wallace a reduced capacity for species-pool recruitment due to line on a fragment of Borneo, as is hypothesised for many stabilised ecological interactions. In one well-studied Asian plants. We compare the morphological and molec-
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