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Metacommunity Analyses Show Increase in Ecological Specialisation 2 Throughout the Ediacaran 3

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Metacommunity Analyses Show Increase in Ecological Specialisation 2 Throughout the Ediacaran 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.05.17.444444; this version posted May 17, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 Metacommunity analyses show increase in ecological specialisation 2 throughout the Ediacaran 3 4 Rebecca Eden1, Andrea Manica1, Emily G. Mitchell1* 5 1Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UK. 6 7 *Correspondence to: [email protected] 8 9 Short title: Metacommunity structuring in the Ediacaran 10 11 Abstract 12 The first animals appear during the late Ediacaran (572 – 541 Ma); an initial diversity increase was 13 followed by a drop, interpreted as catastrophic mass extinction. We investigate the processes 14 underlying these changes using the “Elements of Metacommunity Structure” framework. The oldest 15 metacommunity was characterized by taxa with wide environmental tolerances, and limited 16 specialisation and inter-taxa interactions. Structuring increased in the middle metacommunity, with 17 groups of taxa sharing synchronous responses to environmental gradients, aggregating into distinct 18 communities. This pattern strengthened in the youngest metacommunity, with communities showing 19 strong environmental segregation and depth structure. Thus, metacommunity structure increased in 20 complexity, with increased specialisation and resulting competitive exclusion, not a catastrophic 21 environmental disaster, leading to diversity loss in the terminal Ediacaran, revealing that the complex 22 eco-evolutionary dynamics associated with Cambrian diversification were established in the Ediacaran. 23 24 25 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.05.17.444444; this version posted May 17, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 26 MAIN TEXT 27 28 Introduction 29 One of the most dramatic events in the history of Earth is the sudden appearance of animals in the 30 fossil record during the Ediacaran period (635-541 Ma), after billions of years of microbial life (5,6). 31 Ediacaran anatomies are particularly difficult to compare to modern phyla, which has hampered our 32 understanding of Ediacaran evolution and how Ediacaran organisms relate to the Cambrian Explosion 33 and extant animal phyla (7). Patterns of taxonomic, morphological and ecospace diversity change 34 dramatically during the Ediacaran (8,9), which has led to the suggestion of several evolutionary 35 radiations, corresponding to the Avalon, White Sea and Nama assemblages (5,10–12). These three 36 assemblages are formed by the taxonomic groupings of communities which occupy partially 37 overlapping temporal intervals and water-depths, with no significant litho-taphonomic or 38 biogeographic influence (10,11,13). The oldest assemblage, the Avalon (575-565 Ma), exhibits 39 relatively limited ecological and morphological diversity (8,9), with only limited palaeoenvironmental 40 influence on its composition and taxa interactions (14–17). The White Sea assemblage (558-550 Ma) 41 shows a large increase in morphological diversity, including putative bilaterians, in tandem with a 42 greater ecological diversity (8) and environmental influence (18). The Nama assemblage (549-543 Ma) 43 includes the oldest biomineralizing taxa, and records a decrease in taxonomic diversity (8,19–21). The 44 reduction in taxonomic diversity and community composition complexity between the White Sea and 45 Nama has been suggested to correspond to a post-White Sea extinction around 550 Ma, which 46 eliminated the majority of Ediacaran soft-bodied organisms (12,22–24). 47 48 Previous studies have focused primarily on defining the different assemblages and the underlying 49 causes for the different assemblages (10,11,13), looking at taxonomic and morphological diversity 50 between assemblages (8,25) with little investigation of how the ecological structure within the 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.05.17.444444; this version posted May 17, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 51 assemblages differs. The network structures of Ediacaran body-fossil and trace fossil taxa were 52 compared by Muscente et al. (12) using modularity to compare found networks (and sub-networks 53 which correspond to assemblages) to random networks. However, these prior cluster and network 54 analyses have not assessed the relative frequency of taxa co-occurrences within assemblages; i.e. 55 whether they are were statistically different to what would be expected by random chance, nor 56 compared the ecological structure within each assemblage to known ecological models. 57 58 In this study, we will investigate the structuring mechanisms within these assemblages using three 59 analyses which have not been previous used to investigate Ediacaran macro-ecology. We used a binary 60 presence-absence matrix for 86 Ediacaran localities and 124 taxa, with paleoenvironment, depth, 61 lithology, time and assemblage data from (11,24) (Fig. S1). First, we will use the “Elements of 62 Metacommunity Structure” (EMS) framework to investigate emergent properties of groups of 63 connected communities that may arise from taxa interactions, dispersal, environmental filtering and the 64 interaction of these factors (2–4) (Fig. 1). The EMS framework is a hierarchical analysis which 65 identifies properties in site-by-taxa presence/absence matrices which are related to the underlying 66 processes shaping taxa distributions (4), but to date has limited application to the fossil record (26). 67 Three metacommunity metrics are calculated to determine the structure: Coherence, Turnover, and 68 Boundary Clumping (2–4). The values of these metrics determine where the metacommunity fits within 69 the EMS framework (Fig. 1), with different metric combinations indicating different underlying 70 processes behind the metacommunity structure. Secondly, we will test to determine which pair-wise 71 taxa co-occurrences are significantly non-random, and whether any non-random co-occurrences are 72 positive or negative. Finally, we use reciprocal averaging to ordinate the sites based on their 73 community composition and then correlate the first-axis ranking with depth to test whether within- 74 assemblage community composition is correlated with depth. 75 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.05.17.444444; this version posted May 17, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 76 77 Figure 1: Idealized metacommunity structures. 78 These graphs show taxa abundance patterns in idealized metacommunities of several taxa (represented 79 by different colors) which respond to a latent environmental gradient (they exhibit significant positive 80 Coherence). 81 82 Results 83 First, we pooled all the sites irrespective of their assemblage, in order to test whether the assemblage 84 definitions harbored distinct communities (Fig. 2). When analysing the total dataset, we found positive 85 Coherence, Turnover and Boundary Clumping, characteristic of a Clementsian structured 86 metacommunity (Fig. 3a, Table 1). Site ordination scores were significantly correlated with assemblage 87 (H=57.686, df=2, p<0.001, Appendix Table 4) and depth (H=51.649, df=7, p<0.001, Table S3), 88 indicating that the structuring in the dataset was due to differences in depth or other assemblage- 89 specific characteristics. To further investigate the nature of this structuring, we focused on the pair-wise 90 co-occurrence patterns: virtually all positive associations resulted from taxa specific to the same 91 assemblage (96.8% of positive associations), and all negative associations from taxa found in different 92 assemblages (100% of negative associations). Therefore, our analyses are consistent with previous 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.05.17.444444; this version posted May 17, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 93 studies (11,12) in finding that Ediacaran taxa are highly segregated by assemblage, as well as 94 confirming a role for depth (Table 2) in structuring the assemblages (10,11). At this broad level of 95 analysis, the strong assemblage signal, at least partially dependent on depth specialisations, obscures 96 any other biotic or abiotic pattern. 97 98 Figure 2: Ordinated data table. The assemblage and palaeoenvironment for each locality are given 99 on the left. Right plot shows the incidence matrix for taxa (columns) for all sites (rows) along the 100 inferred environmental gradient after ordination. Ordination was calculated according to occurrence 101 resulting from the overall metacommunity analysis. The presence of a taxon is given by a colored
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