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The Relative Influence of Niche Versus Neutral Processes on Ediacaran Communities

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The Relative Influence of Niche Versus Neutral Processes on Ediacaran Communities bioRxiv preprint doi: https://doi.org/10.1101/443275; this version posted December 10, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 The relative influence of niche versus neutral processes on Ediacaran communities 2 3 *Emily G .Mitchell1, Simon Harris2, Charlotte G. Kenchington1, Philip Vixseboxse3, Lucy 4 Roberts4, Catherine Clark1, Alexandra Dennis1, Alexander G. Liu1, Philip R. Wilby2. 5 6 1Department of Earth Sciences, University of Cambridge, Downing Street, Cambridge CB2 7 3EQ, UK. 8 2British Geological Survey, Nicker Hill, Keyworth, Nottingham NG12 5GG, United 9 Kingdom. 10 3School of Earth Sciences, University of Bristol, Wills Memorial Building, Queens Road, 11 Bristol, BS8 1RJ, United Kingdom. 12 4Department of Zoology, University of Cambridge… 13 14 *Correspondence: [email protected]. 15 16 Keywords: Ediacaran, neutral theory, spatial point process analysis, paleoecology, ecology, 17 paleontology, rangeomorph 18 19 1 bioRxiv preprint doi: https://doi.org/10.1101/443275; this version posted December 10, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 20 Abstract 21 A fundamental question in community ecology is the relative influence of niche versus 22 neutral processes in determining ecosystem dynamics. The extent to which these processes 23 structured early animal communities is yet to be explored. Here we use spatial point process 24 analyses (SPPA) to determine the influence of niche versus neutral processes on early total- 25 group metazoan paleocommunities from the Ediacaran Period ~565 million years in age. 26 Preservation of these sessile organisms in large in-situ populations on exposed bedding 27 planes enables inference of the most likely underlying processes governing their spatial 28 distributions by SPPA. We conducted comprehensive spatial mapping of six of the largest 29 Ediacaran paleocommunities in Newfoundland, Canada and Charnwood Forest, UK using 30 LiDAR, photogrammetry and a laser-line probe. For each paleocommunity we determined 31 the best-fit spatial model for each univariate and bivariate species distribution, comparing 32 four sets of spatial models (complete spatial randomness, dispersal, habitat, and combined 33 dispersal with habitat) using goodness-of-fit tests. Random and dispersal models are 34 considered neutral processes while habitat and combined models are considered niche 35 processes. We find the dynamics of these paleocommunities to be dominated by neutral 36 processes, with limited influence from niche processes. Our findings are consistent with 37 community model predictions of when neutral dynamics dominate, but are in stark contrast to 38 the niche-dominated communities of the modern marine realm. Thus, while the underlying 39 processes determining metazoan community assembly appear to have been in place since the 40 appearance of the first macroscopic, complex animals, the dynamics of these early metazoan 41 communities were fundamentally different to those of extant communities. 42 2 bioRxiv preprint doi: https://doi.org/10.1101/443275; this version posted December 10, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 43 Significance statement 44 The extent to which habitat and dispersal processes structure the earliest animal communities 45 found during the Ediacaran Period ~565 million years ago, is unknown. In this study we 46 analyse six of the largest and most diverse fossil assemblages from Newfoundland, Canada 47 and Charnwood Forest, UK, using spatial point processes analyses to determine the relative 48 influence of habitat processes (niche) and dispersal processes (neutral) on the spatial 49 distribution of taxa. The vast majority of Ediacaran taxon distributions were controlled by 50 neutral processes, in striking contrast to niche-dominated modern marine ecosystems, but 51 consistent with model predictions of when neutral dynamics dominate communities. Thus 52 the underlying processes determining metazoan community assembly have been in place 53 since the appearance of the first macroscopic, complex animals. 54 3 bioRxiv preprint doi: https://doi.org/10.1101/443275; this version posted December 10, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 55 Two opposing theories lie at the centre of debate regarding the fundamental dynamics that 56 govern ecosystem structure and biodiversity: niche and neutral. Niche theory is a central 57 tenet of classical ecological theory, whereby species avoid competitive exclusion by 58 occupying different niches within the ecosystem (MacArthur 1984). The smaller the niche 59 overlap, the less competition occurs between taxa, allowing more taxa to exist in an area 60 without driving each other to extinction. Species are able to co-exist because they are 61 different. Niche models describe selection-dominated ecosystems, whereby species 62 dynamics operate deterministically as a series of inter-specific interactions, which act as 63 stabilizing mechanisms for the ecosystem (Adler et al. 2007). 64 65 Neutral processes are often referred to as the null model of niche processes: instead of species 66 differences enabling co-existence, their similarity drives high diversity (Hubbell 2001). 67 Within neutral models, species fitness is constant, and so different taxa can co-exist because 68 none has a significant competitive advantage over the other. Despite this seemingly highly 69 unrealistic assumption, neutral theories have been able to accurately reproduce certain 70 species-area-distributions (SADs; Hubbell 2001); sometimes better than niche theories; 71 (MacArthur 1984), as well as SAD and beta diversity patterns (Condit et al. 2002, Chisholm 72 et al. 2010). 73 74 Unified or continuous theories, whereby niche and neutral processes combine to generate 75 species coexistence (Grave et al. 2004, Adler et al. 2007), have emerged in recent years. In 76 these combined models, species can exhibit strong differences and strong stabilizations 77 (niche-type), or weak stabilizations because of similar fitness (neutral-type), with classic 78 niche and neutral models the extreme endmembers of this continuum model. However, it is 79 often not possible to analytically determine whether the niche or neutral model fits the data 4 bioRxiv preprint doi: https://doi.org/10.1101/443275; this version posted December 10, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 80 better, making it hard to untangle the relative influence of niche and neutral-type processes 81 within modern complex ecosystems. 82 83 In order to investigate whether niche or neutral processes were the most important during the 84 first establishment of modern-style ecosystems, we focus on some of the oldest known total- 85 group metazoan communities: those comprising the Ediacaran macrobiota, dated to ~571-560 86 million years in age (Droser et al., 2017). The evolution of macroscopic metazoans was 87 coupled with a transformation in ecosystem dynamics. Paleocommunities evolved from the 88 assumed simple community structure of pre-Ediacaran microbial populations (Butterfield 89 2007), through the Ediacaran paleocommunities that exhibited both simple and complex 90 community structures (Darroch et al. 2018), and on into the Cambrian ‘modern’ metazoan 91 ecosystems with a similar ecosystem structure to the present (Dunne et al. 2008). 92 93 The oldest metazoan-dominated communities form part of the Avalonian Assemblage of the 94 Ediacara Biota (Waggoner 2003), and are known primarily from Newfoundland, Canada and 95 Leicestershire, UK. Avalonian soft-bodied organisms were preserved in-situ in deep-water 96 strata dated to ~572-560 Ma (Pu et al. 2016, Noble et al. 2016), beneath volcanic ash-rich 97 event beds (Wood et al. 2003, Narbonne 2005). As such, exposed bedding-plane surfaces 98 preserve near-complete censuses of the communities (Wood et al. 2003, Clapham et al. 99 2003); though the impact of erosion of these surfaces needs to be taken into account 100 (Matthews et al. 2017), cf. Mitchell et al. 2015). Since they were soft bodied, dead organisms 101 could not accumulate over long time periods, removing problems associated with time- 102 averaging of the paleocommunity. Furthermore, Avalonian ecosystems pre-date macro- 103 predation and vertical burrowing, such that upon death, organisms were not eaten and 104 remained in place. As a result, and because the organisms are considered to have been non- 5 bioRxiv preprint doi: https://doi.org/10.1101/443275; this version posted December 10, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 105 mobile, each individual bedding plane is interpreted to record organisms that lived 106 contemporaneously, with recently deceased and decaying organisms being the primary 107 recognised record of identifiable time-averaging (Liu et al. 2011; Mitchell and Butterfield 108 2018; see also Wilby et al. 2015). 109 110 Consequently, the position
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