Ecological Speciation in Darkness? Spatial Niche Partitioning in Sibling Subterranean Spiders (Araneae: Linyphiidae: Troglohyphantes)
Total Page：16
File Type：pdf, Size：1020Kb
AperTO - Archivio Istituzionale Open Access dell'Università di Torino Ecological speciation in darkness? Spatial niche partitioning in sibling subterranean spiders (Araneae: Linyphiidae: Troglohyphantes) This is the author's manuscript Original Citation: Availability: This version is available http://hdl.handle.net/2318/1676419 since 2019-03-08T12:15:43Z Published version: DOI:10.1071/IS17090 Terms of use: Open Access Anyone can freely access the full text of works made available as "Open Access". Works made available under a Creative Commons license can be used according to the terms and conditions of said license. Use of all other works requires consent of the right holder (author or publisher) if not exempted from copyright protection by the applicable law. (Article begins on next page) 07 October 2021 Invertebrate Systematics Ecological speciation in darkness? Spatial niche partitioning in sibling subterranean spiders (Araneae: Linyphiidae: Troglohyphantes) Journal:For Invertebrate Review Systematics Only Manuscript ID IS17090.R2 Manuscript Type: Research paper Date Submitted by the Author: 02-Mar-2018 Complete List of Authors: Mammola, Stefano; Universita degli Studi di Torino, Department of Life sciences and systems Biology Arnedo, Miquel; Facultat de Biologia, Universitat de Barcelona, Biologia Animal Pantini, Paolo; Museo civico di Scienze Naturali “E. Caffi” Piano, Elena; Universita degli Studi di Torino, Department of Life sciences and systems Biology Chiappetta, Nicolò; Universita degli Studi di Torino, Department of Life sciences and systems Biology Isaia, Marco; Universita degli Studi di Torino, Department of Life sciences and systems Biology Araneae, evolution, functional morphology, phylogeny, species boundaries, Keyword: species delineation, subterranean, soil, molecular taxonomy, mitochondrial DNA Note: The following files were submitted by the author for peer review, but cannot be converted to PDF. You must view these files (e.g. movies) online. FIGURE 1.odp FIGURE 2.odp FIGURE 4.odp http://www.publish.csiro.au/journals/is Page 1 of 46 Invertebrate Systematics 1 Ecological speciation in darkness? Spatial niche partitioning in sibling 2 subterranean spiders (Araneae: Linyphiidae: Troglohyphantes) 3 4 Stefano Mammola1, Miquel A. Arnedo2, Paolo Pantini3 , Elena Piano1, Nicolò Chiappetta1, Marco 5 Isaia1,* 6 7 1) Department of Life Sciences and Systems Biology, University of Turin, Turin, Italy. 8 2) Department of Evolutionary Biology, Ecology and Environmental Sciences & Biodiversity 9 Research Institute, University of Barcelona, Barcelona, Spain. 10 3) Museo civico di ScienzeFor Naturali Review “E. Caffi”, Bergamo, Only Italy. 11 *Corresponding author: [email protected] 12 13 Author contribution statement 14 EP, MI and SM performed fieldwork in the Pugnetto hypogean complex. EP sorted biological 15 specimens collected in the subterranean sampling devices. SM and MI described the new species. 16 NC measured specimens for the ecological analysis. SM analysed ecological data. SM and MI 17 wrote the first draft of the paper. MA conducted the analyses of the molecular data and wrote the 18 relative sections. PP supervised the preparation of morphological drawings, provided specimens 19 stored in the museum collection and revised the species description. All authors contributed to the 20 writing of the paper trough discussions and additions to the text. 21 22 Conflict of Interest statement 23 The authors declare no conflicts of interest. 24 25 26 27 1 http://www.publish.csiro.au/journals/is Invertebrate Systematics Page 2 of 46 28 Abstract 29 Speciation in subterranean habitats is commonly explained as the result of divergent selection in 30 geographically isolated populations; conversely, the contribution of niche partitioning in driving 31 subterranean species diversification has been rarely quantified. We integrated molecular and 32 morphological data with a hypervolume analysis based on functional traits to study a potential case 33 of parapatric speciation by means of niche differentiation in two sibling spiders inhabiting 34 contiguous subterranean habitats within a small alpine hypogean site. Troglohyphantes giachinoi n. 35 sp. and T. bornensis are diagnosed by small details of the genitalia, which are likely to be involved 36 in a reproductive barrier. Molecular analysis recovered the two species as sister, and revealed a 37 deep genetic divergence that may trace back to the Messinian (~6 My ago). The hypervolume 38 analysis highlighted a marginalFor overlap Review in their ecological Only niches, coupled with morphological 39 character displacement. Specifically, T. giachinoi n. sp. exhibits morphological traits suitable for 40 thriving in the smaller pores of the superficial network of underground fissures (MSS), whereas T. 41 bornensis shows a higher adaptation to the deep subterranean habitat. Our results suggest that 42 different selective regimes within the subterranean environment, i.e. deep caves versus MSS, may 43 either drive local speciation or facilitate contiguous distributions of independently subterranean 44 adapted species. 45 46 Table of Contents (TOC) abstract 47 Although speciation is most often explained as the result of divergent selection in geographically 48 isolated populations, alternative evolutionary scenarios have been documented by scientists. We 49 describe how two sibling spiders may have originated via ecological differentiation in two 50 contiguous and interconnected subterranean habitat with different size of void spaces. Our data 51 demonstrates that habitat size may drive species differentiation within the subterranean realm, by 52 minimizing intraspecific competition through niche partitioning, and provides further evidence of 53 the importance of space heterogeneity as an evolutionary driver. 54 55 56 57 58 59 60 2 http://www.publish.csiro.au/journals/is Page 3 of 46 Invertebrate Systematics 61 Introduction 62 While allopatric speciation — divergence with geographic isolation — is the most common process 63 originating biological diversity (Coyne and Orr 2004), a body of evidence indicate that species 64 divergence may occasionally occur with limited or even without geographical isolation — 65 parapatric and sympatric speciation, respectively (Futuyma and Mayer 1980; Tregenza and Butlin 66 1999; Gavrilets 2003; Jiggins and Chris 2006; Bolnik and Fitzpatrick 2007). For instance, such 67 speciation processes have been observed in fruit flies (Filchak et al. 2000), palm trees (Savolainen 68 et al. 2006) and cichlid fish (Berluenga et al. 2006; Gavrilets et al. 2007). Parapatric and sympatric 69 mode of speciation are often the result of ecologically-based divergent selection, i.e. ecological 70 speciation (Mayr 1942, 1947). Three main ecological drivers of divergent selection leading to 71 speciation have been putFor forward inReview literature (Rundle andOnly Nosil 2005; Schluter and Conte 2009): 72 sexual selection (Panhuis et al. 2001; Kirkpatrick and Ravigné 2002), species interaction (Schluter 73 2000), and environmental differentiation (Schluter 2000, 2001). The latter mechanism is probably 74 the best documented and understood, and can occur when two populations occupy distinct 75 ecological niches — here intended as the set of environmental conditions and/or functional traits 76 maximizing the fitness of a certain species — and hence are subJect to two different selective 77 regimes, within the same habitat (Rundle and Nosil 2005). 78 Since the beginning of modern subterranean biology in the 1900's, researchers have 79 recognized the subterranean domain as a well-suited system in which to test eco-evolutionary 80 theories, especially those related to the processes of convergent (Jones et al. 1992; Wiens et al. 81 2003; Wilcox et al. 2004; Juan et al. 2010; Protas and Jeffery 2012; Gonzalez et al. 2018) and 82 regressive evolution (Heuts 1953; Porter and Crandall 2003; Jeffery 2009; Rétaux and Casane 2013; 83 Klaus et al. 2013). Also, subterranean habitats represent ideal model systems in which to study 84 allopatric speciation. Most caves are indeed regarded as "islands" surrounded by inhospitable 85 habitats (e.g., Culver 1970a, 1971, Snowman et al. 2010; Esposito et al. 2015; Fattorini et al. 2016), 86 resulting in low gene flow among cave populations (e.g. Caccone 1985; Mammola et al. 2015b; 87 Weckstein et al. 2016) and frequent speciation events connected to this geographic isolation (Barr 88 and Holsinger 1985). This pattern is empirically confirmed by the documented higher proportion of 89 subterranean endemic species relative to their surface counterparts (e.g., Sharratt et al. 2000; 90 Christman et al. 2005; Cardoso 2012; Niemiller and Zigler 2013; Wynne et al. 2014). Nevertheless, 91 mechanisms other than geographic isolation have been sometime invoked to explain the origin of 92 subterranean organisms (Juan et al. 2010). Niche-based processes, for example, may play a key role 93 in shaping subterranean species diversity (e.g., Culver 1970b; Fišer C. et al. 2012, 2015; Fišer Z. et 3 http://www.publish.csiro.au/journals/is Invertebrate Systematics Page 4 of 46 94 al. 2015), whereas parapatric or even sympatric speciation modes may explain the origin of certain 95 taxa, such as the Astyanax cave fishes from Mexico (Wilkens and Hüppop 1986; Strecker et al. 96 2012), the Tennessee cave salamanders (Niemiller et al. 2008; also discussed in Nosil 2008), the 97 subterranean diving beetles from Australia (Cooper et al. 2002; Leys et al. 2003; Leys and