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Role of Seed Size, Phenology, Oogenesis and Host Distribution In View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Diposit Digital de Documents de la UAB Integrative Zoology 2018; 13: 267–279 doi: 10.1111/1749-4877.12293 1 ORIGINAL ARTICLE 1 2 2 3 3 4 4 5 5 6 6 7 Role of seed size, phenology, oogenesis and host distribution in the 7 8 8 9 specificity and genetic structure of seed weevils Curculio( spp.) in 9 10 10 11 mixed forests 11 12 12 13 13 14 Harold ARIAS-LECLAIRE1,2 Raúl BONAL,3,4 Daniel GARCÍA-LÓPEZ5 and Josep Maria 14 15 1 15 16 ESPELTA 16 17 1CREAF, Centre for Ecological Research and Forestry Applications, Cerdanyola del Vallès, 08193, Spain, 2Exact and Natural 17 18 Sciences School, State Distance University of Costa Rica, UNED, Mercedes de Montes de Oca, San José, Costa Rica, 3Forest 18 19 19 Research Group, INDEHESA, University of Extremadura, Plasencia, Spain, 4DITEG Research Group, University of Castilla-La 20 20 Mancha, Toledo, Spain and 5Zoology Department, Autonomous University of Barcelona, Cerdanyola del Vallès, Spain 21 21 22 22 23 23 24 Abstract 24 25 25 26 Synchrony between seed growth and oogenesis is suggested to largely shape trophic breadth of seed-feeding in- 26 27 sects and ultimately to contribute to their co-existence by means of resource partitioning or in the time when in- 27 28 festation occurs. Here we investigated: (i) the role of seed phenology and sexual maturation of females in the 28 29 host specificity of seed-feeding weevils (Curculio spp.) predating in hazel and oak mixed forests; and (ii) the 29 30 consequences that trophic breadth and host distribution have in the genetic structure of the weevil populations. 30 31 DNA analyses were used to establish unequivocally host specificity and to determine the population genetic 31 32 structure. We identified 4 species with different specificity, namely Curculio nucum females matured earlier and 32 33 infested a unique host (hazelnuts, Corylus avellana) while 3 species (Curculio venosus, Curculio glandium and 33 34 Curculio elephas) predated upon the acorns of the 2 oaks (Quercus ilex and Quercus pubescens). The high spec- 34 35 ificity of C. nucum coupled with a more discontinuous distribution of hazel trees resulted in a significant genet- 35 36 ic structure among sites. In addition, the presence of an excess of local rare haplotypes indicated that C. nucum 36 37 populations went through genetic expansion after recent bottlenecks. Conversely, these effects were not ob- 37 38 served in the more generalist Curculio glandium predating upon oaks. Ultimately, co-existence of weevil spe- 38 39 cies in this multi-host-parasite system is influenced by both resource and time partitioning. To what extent the 39 40 restriction in gene flow among C. nucum populations may have negative consequences for their persistence in a 40 41 time of increasing disturbances (e.g. drought in Mediterranean areas) deserves further research. 41 42 42 Key words: Corylus avellana, Curculio spp., genetic structure, Quercus spp., trophic breadth 43 43 44 44 45 45 46 46 47 INTRODUCTION 47 48 48 49 Correspondence: Josep Maria Espelta, CREAF, Cerdanyola del Seed predation by insects may play a crucial role in 49 50 Vallès, Spain. plant population dynamics, by reducing the reproductive 50 51 Email: [email protected] output (Bonal et al. 2007; Espelta et al. 2008) and con- 51 © 2017 The Authors. Integrative Zoology published by International Society of Zoological Sciences, 267 Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd 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. H. Arias-LeClaire et al. 1 straining the regeneration process (Espelta et al. 2009b). seeds of different hosts in multi-specific systems has 1 2 Trophic breadth and specificity of seed-feeding insects been seldom explored. 2 3 is often explained by differences among plant hosts in The breadth of the trophic niche of seed-feeding in- 3 4 chemical or morphological traits (Bernays & Graham sects (specialist vs generalist) may influence the num- 4 5 1988; Forister et al. 2015). Differences in phytochemis- ber of species that predate upon different seeds and it 5 6 try (mainly nitrogen-based defensive compounds) have has consequences for the dynamics of the communi- 6 7 been observed to be highly relevant for the diversifi- ty of hosts (Espelta et al. 2009b). However, beyond the 7 8 cation of phytophagous insects and their diet breadth effects on plant fitness, differences in the trophic niche 8 9 (Kergoat et al. 2005). Concerning other seed features, may also influence the population dynamic of the seed 9 10 size is a trait claimed to influence ecomorphological di- consumers (Ylioja et al. 1999) depending on life-his- 10 11 versification in many endophytic insects (e.g. body size tory traits such as dispersal ability and landscape attri- 11 12 and rostrum shape), promoting differences in their tro- butes (i.e. abundance and spatial distribution of hosts). 12 13 phic niche, ecological adaptations and species radiation Spatial connectivity among plant-hosts has been shown 13 14 (Hughes & Voegler 2004a; Bonal et al. 2011; Pegue- to be especially relevant for insects with low disper- 14 15 ro et al. 2017). In addition to chemical and morpholog- sal ability (Thomas et al. 2001; Kruess 2003), resulting 15 16 ical differences, seeding phenology and stochasticity in a stronger genetic structure and reduced gene flow in 16 17 in the availability of this resource have also been sug- the insect populations located on more isolated hosts. In 17 18 gested as key factors influencing the guild of insect spe- the long run, host isolation may even result in coloni- 18 19 cies predating upon a particular plant host (Espelta et zation credits for some insect species, especially those 19 20 al. 2008, 2009b; Coyle et al. 2012; see also Pélisson et with a narrower diet breadth (Ruiz-Carbayo et al. 2016) 20 21 al. 2013a). As insects are short-living organisms, syn- and poor dispersal ability (Pélisson et al. 2013b; Hei- 21 22 chronization of their life-cycle with the resources upon neger et al. 2014). Conversely, generalist species may 22 23 which they depend is critical (Bale et al. 2002, 2007; show a more continuous distribution in the landscape, 23 24 Hood & Ott 2010). Therefore, processes such as adult benefiting from the spatial overlap of the different host 24 25 emergence (Espelta et al. 2017) and oogenesis (Trudel plants upon which they feed (Newman & Pilson 1997), 25 26 et al. 2002; Son & Lewis 2005) have to be tightly con- and show no genetic structure differences among popu- 26 27 nected with the presence of seeds for oviposition (Bonal lations owing to gene flow. Interestingly, for seed-feed- 27 28 et al. 2010). In particular, oogenesis (i.e. egg maturation ing insects a comparison of the genetic structure of their 28 29 in females) has been predicted to differ depending on populations and the spatial structure of their potential 29 30 the stochasticity of seeds availability. Thus, proovigen- hosts could provide strong evidence about differences 30 31 esis (i.e. females have already mature eggs at the onset of the trophic niche breadths. Moreover, the use of mo- 31 32 of their adult life) would be favored in species predating lecular techniques (DNA barcoding) may help to detect 32 33 upon hosts that regularly produce seeds while synovi- cryptic speciation and trophic niche segregation among 33 34 genesis (i.e. females start their adult life with imma- morphologically similar species (Peguero et al. 2017), 34 35 ture eggs) would be advantageous for species exposed and also to establish species specificity in an unequiv- 35 36 to more random fluctuations of seed production (Jervis ocal way in comparison to classifications based on the 36 37 et al. 2008; Richard & Casas 2009), as they can better presence or absence of a species on a particular plant, 37 38 adjust the amount of energy invested in reproduction to especially when the lack of morphological differences 38 39 the amount of seeds (but see Pélisson 2013b). Ultimate- at certain stages (e.g. larvae) make species identification 39 40 ly, the co-existence of the different seed consumers in impossible otherwise (Govindan et al. 2012). Unfortu- 40 41 a multi-host community could be mediated by resource nately, this combination of landscape ecology (i.e. host 41 42 partitioning (e.g. insects predate preferentially upon dif- connectivity) and population genetics when studying the 42 43 ferent species according to different seed traits; see Es- breadth of the trophic niche and dispersal ability of phy- 43 44 pelta et al. 2009a), time-partitioning (e.g. insects exhibit tophagous insects remains largely unexplored. 44 45 45 differences in life span and the timing of seed predation; The main aims of this study have been to investigate 46 46 see Pélisson et al. 2012) or the trade-off among disper- in a multi-host and multi-seed-predator system the role 47 47 sal versus dormancy ability to cope with resource scar- of seed size, seed phenology and ooegenesis in the host 48 48 city (Pélisson et al. 2012). Yet, the importance of the specificity of seed-parasite weevils (Curculio spp.) and 49 49 interplay among seed size, seeding phenology and oo- to analyze the consequences that potential differences 50 50 genesis in driving the guild of insects predating upon in trophic specialization and host distribution may have 51 51 268 © 2017 The Authors.
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