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Metacommunity analyses show an increase in ecological specialisation throughout the Ediacaran period

['Rebecca Eden', 'Department Of Zoology', 'University Of Cambridge', 'Cambridge', 'United Kingdom', 'Andrea Manica', 'Emily G. Mitchell']

Date: 2022-05

The first animals appear during the late Ediacaran (572 to 541 Ma); an initial diversity increase was followed reduction in diversity, often interpreted as catastrophic mass extinction. We investigate Ediacaran ecosystem structure changes over this time period using the “Elements of Metacommunity Structure” framework to assess whether this diversity reduction in the Nama was likely caused by an external mass extinction, or internal metacommunity restructuring. The oldest metacommunity was characterised by taxa with wide environmental tolerances, and limited specialisation or intertaxa associations. Structuring increased in the second oldest metacommunity, with groups of taxa sharing synchronous responses to environmental gradients, aggregating into distinct communities. This pattern strengthened in the youngest metacommunity, with communities showing strong environmental segregation and depth structure. Thus, metacommunity structure increased in complexity, with increased specialisation and resulting in competitive exclusion, not a catastrophic environmental disaster, leading to diversity loss in the terminal Ediacaran. These results reveal that the complex eco-evolutionary dynamics associated with Cambrian diversification were established in the Ediacaran.

Introduction

One of the most dramatic events in the history of Earth is the sudden appearance of animals in the fossil record during the Ediacaran period (635 to 541 Ma), after billions of years of microbial life [1–3]. Ediacaran anatomies are particularly difficult to compare to modern phyla, which has hampered our understanding of Ediacaran evolution and how Ediacaran organisms relate to the Cambrian Explosion and extant animal phyla [4]. Patterns of taxonomic, morphological, and ecospace diversity change dramatically during the Ediacaran [5,6], which has led to the suggestion of several evolutionary radiations, corresponding to the Avalon, White Sea, and Nama assemblages [1,7–9]. These 3 assemblages consist of groupings of communities that occupy partially overlapping temporal intervals and water depths, with no significant litho-taphonomic or biogeographic influence [7,8,10]. The oldest assemblage, the Avalon (575 to 565 Ma), exhibits relatively limited ecological and morphological diversity [5,6], with only limited palaeoenvironmental influence on its composition and taxa interactions [11–14]. The White Sea assemblage (558 to 550 Ma) shows a large increase in morphological diversity, including putative bilaterians [5], in tandem with a greater ecological diversity that includes the appearance of grazing, herbivory, and widespread motility [15,16]. These innovations are coupled to the development of dense communities with high community heterogeneity between environments [16,17] and increased taxa sensitivity to fine-scale environment [12,18]. The Nama assemblage (549 to 543 Ma) includes the oldest biomineralising taxa and records a decrease in taxonomic diversity [5,19–21]. This reduction in taxonomic diversity, sometimes referred to as the “diversity drop,” has been suggested to correspond to a post-White Sea extinction around 550 Ma, which eliminated the majority of Ediacaran soft-bodied organisms [9,22–24]. This diversity drop has been suggested to be caused by either an environmental driven catastrophic environmental extinction or biotic replacement driven extinction [9,21,23,24]. Recent work has shown that a biotic replacement driven extinction, whereby mobile metazoans outcompeted soft-bodied Ediacaran organisms through bioturbation and ecosystem engineering, is unlikely, due in part to prolonged co-occurrence of trace fossils with soft-bodied biota [1,25]. Other currently unknown and/or unpreserved intrinsic causes behind a biotic replacement model cannot be excluded at the moment.

Previous studies have focused primarily on defining the different assemblages and what the underlying factors behind the different assemblages [7,8,10], looking at taxonomic and morphological diversity between assemblages [5,26] with little investigation of how the ecological structure within the assemblages differs. The network structures of the co-occurrence of Ediacaran body fossil and trace fossil taxa were compared by Muscente and colleagues [9] who found compartmentalisation of the assemblages within the total Ediacaran network. However, the prior cluster analyses of [7,8,10] and network analyses of [9] have not assessed the relative frequency of taxa co-occurrences within assemblages; i.e., whether they were statistically different to what would be expected by random chance, nor compared the ecological structure within each assemblage to known ecological models.

In this study, we will investigate the structural attributes within these assemblages using 3 analyses that have not previous been used to investigate Ediacaran macroecology. We used presence–absence data encompassing 86 Ediacaran localities and 124 taxa, with paleoenvironment, depth, lithology, time, and assemblage data from [8,24] (S1 Fig). Ediacaran fossils are commonly found preserved in situ, so their bedding planes (the rock surfaces that preserve the fossils) preserve near-compete censuses of the communities [15,27]. This exceptional preservation means that ecological analyses normally reserved for modern communities can be applied (e.g., [12,28]).

First, we will use the “Elements of Metacommunity Structure” (EMS) framework to investigate emergent properties of groups of connected communities that may arise from taxa interactions, dispersal, environmental filtering, and the interaction of these factors [29–31] (Fig 1). Most fossil metacommunities do not fulfil the requirements of random sampling that would be needed to analyse them with such an ecological framework. However due to their exceptional preservation, the Ediacaran metacommunities are an exceptional census of the benthic assemblages present at the time, making them amenable to be analysed within the EMS framework. EMS does not assume even dispersal across all sites, with intermediate levels of disturbance associated with the highest levels of filtering of community by biotic and abiotic factors [29], and dispersal limitation associated with negative turnover [32]. Ediacaran communities vary in how much they are separated in time and space, from ecological to geological time scales [8,9,13], and their organisms have been shown to have large dispersal ranges based on reproductive mode [28,33,34] and species occurrence over large space and time scales [35]. Because the connectivity of these Ediacaran communities via dispersal has been established, here we define metacommunities as sets of fossil localities (communities), which are connected by the dispersal of many species [29]. The EMS framework is a hierarchical analysis that identifies properties in site-by-taxa presence/absence matrices, which are related to the underlying processes shaping taxa distributions [31], but to date has limited application to the fossil record [36]. Three metacommunity metrics are calculated to determine the structure: coherence, turnover, and boundary clumping [29–31], which are hierarchical rather than independent of each other. The values and statistical significance of these metrics determine where the metacommunity fits within the 14 different metacommunity types within the EMS framework (Fig 1), with different metric combinations indicating different underlying processes behind the metacommunity structure. To determine whether an observed metric score differs significantly from random, we computed the z-score, which measures its distance from the mean of the randomisations (simulation mean) as the number of standard deviations (thus making it comparable across metrics with difference units). If the z-score is negative, the observed value is smaller than the simulated mean; if it is positive, then it is greater than the simulated mean; z ≥ │3│ indicates a significant deviation.

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TIFF original image Download: Fig 1. Idealised metacommunity structures adapted from [ Idealised metacommunity structures adapted from [ 30 ]. These graphs show taxa abundance patterns in idealised metacommunities of several taxa (represented by different colours), which respond to a latent environmental gradient (they exhibit significant positive coherence). The first step of the analyses (START) is to determine whether the metacommunity exhibits positive, negative, or random coherence. Random coherence corresponds to NS metacommunity structure; negative coherence is a checkerboard pattern [45], so significant mutual exclusivity between species and sites. Positive coherence indicates mutual co-occurring taxa associations, and there are several different possible models. For positive coherence, turnover and boundary clumping are calculated to determine the type of metacommunity structure. Nonsignificant turnover corresponds to quasi structures. These EMF analyses enable the structure of metacommunities to be grouped into one of 14 models: (1) random; (2) checkerboard; (3–5) nested clumped, random, and hyperdispersed; (6–8) Clementsian, Gleasonian, and evenly spaced; (9–10) Quasi nester clumped and hyperdispersed; and (11–12) quasi Clementsian and evenly spaced. See S1 Table. EMF, Elements of Metacommunity Framework; NS, no significant. https://doi.org/10.1371/journal.pbio.3001289.g001

Coherence is a measure of the extent to which all the taxa respond to the same environmental gradient, where this gradient may result from the interplay of several biotic and abiotic factors that differ between sites [37]. Coherence is positive when the taxa in the site-by-taxa matrix all respond to the same environmental gradient. Most extant well-sampled metacommunities display significant positive coherence due to similarities in evolutionary history, ecological preferences, or life history trade-offs within communities [37]. A significant negative coherent site-by-taxa matrix reflects a high number of mutually exclusive taxa pairs creating checkerboard patterns [7,9,10]. These checkerboard patterns do not have further underlying structure (in contrast to positive coherence patterns; Fig 1), as there is no discernible gradient to which all the taxa respond. Negative co-occurrences and significant segregation/checkerboard patterns can be formed from strong competition, grazing/herbivory, or strongly nonoverlapping niches, all of which form similar metacommunity patterns due the presence of mutually exclusive pairs of taxa [29,31,37]. A nonsignificant coherence reflects no significant metacommunity structuring (Fig 1). For metacommunities that have positive coherence, the turnover metric tests the amount of taxa replacement between sites [38]. If taxa ranges are nested within each other, there is less turnover than expected by chance along the gradient (significantly negative). If there are more differences in site taxa composition along the gradient than expected by chance, turnover is significantly positive and the structure is nonnested. Nonsignificant turnover indicates a weaker structuring mechanism, termed a quasi structure (Fig 1) [30]. Quasi structures have the same fundamental characteristics as the idealised structures, but because range turnover is not significantly different from random, it is likely that the underlying structuring mechanisms are weaker than those for which turnover is significant. The final metric, boundary clumping measures the extent to which taxa range limits cluster at the same sites across the environmental gradient [37]. The range limits can be clumped (significant positive), hyperdispersed (significant negative), or random (nonsignificant).

Positive coherence and negative turnover result in nested metacommunities with taxa-poor sites being predictable subsets of taxa-rich sites, implying that species are dispersal limited [39]. Nested metacommunities have been shown to be associated with a low degree of spatial connectivity and environmental variation [39] and have been shown to govern postextinction dynamics [40].

Clumped species boundaries tend to be associated with the transitions between different biomes, where 2 biological communities mix, in contrast to hyperdispersed species loss where species loss is evenly distributed across the range [30]. Positive coherence and turnover with hyperdispersed (negative) boundary clumping describes an evenly spaced metacommunity (Fig 1). Where coherence, turnover and boundary clumping are all positive, the metacommunity is classed as Clementsian (Fig 1), where groups of taxa with similar range boundaries co-occur and respond in a similar way to environment gradients [37,41]. Taxa within Clementsian metacommunities respond synchronously to environmental gradients, suggesting physiological or evolutionary trade-offs associated with environmental thresholds [42], tend to result from high levels of environmental variability and spatial connectivity [39], and are found to be the most common (e.g., [32]). When coherence and turnover are positive but there is no significant boundary clumping, the metacommunity is described as Gleasonian (Fig 1) where each taxon reacts individualistically to environmental gradients [30].

Secondly, we used Spearman rank correlations to test whether within-assemblage community composition is correlated with depth. The ordering of the sites was given by the ordination output from the EMS analyses (Fig 2), which is produced by reciprocal averaging, a type of correspondence analysis that ordinates the sites (y-axis of Fig 2) based on their species composition (x-axis of Fig 2) [31]. This ordering groups the sites together with similar community composition, and we can see from Fig 2 that the assemblages (indicated by different colours) are grouped together and that the depths (shown alongside the y-axis) show a correspondence with these assemblages, with the Avalon sites deeper, then increased shallowing up the y-axis and ordination with the Nama sites being the most shallow. This first-axis ranking of the sites was used to test whether there was a significant association with depth.

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TIFF original image Download: Fig 2. Ordinated data table. The assemblage and palaeoenvironment for each locality are given on the left. Sites are ranked based on reciprocal averaging ordination. Right plot shows the incidence matrix for taxa (columns) for all sites (rows) along the inferred environmental gradient after ordination. Ordination was calculated according to occurrence resulting from the overall metacommunity analysis. The presence of a taxon is given by a coloured square, absence by white. Doushantuo and indeterminate sites were excluded from the assemblage-level analyses. Depth index indicates the relative depth of the locality (cf., [8]), as determined by palaeoenvironment. The data underlying this Figure can be found in 10.6084/m9.figshare.13664105"https://doi.org/10.5061/dryad.1mh30 and in S1 Data. https://doi.org/10.1371/journal.pbio.3001289.g002

Thirdly, we will test to determine which pairwise taxa co-occurrences are significantly nonrandom, and whether any nonrandom co-occurrences are positive or negative. We use a combinatorics approach to test whether species pairs are randomly distributed among sites [43]. If co-occurrences are significantly nonrandom, this suggests a shared underlying ecological or evolutionary process. While the interpretation of co-occurrence data is complicated because co-occurrence does not necessarily correspond to interaction [44], here we interpret pairwise correlations (or associations) to within the wider EMS framework where co-occurrences are not taken necessarily as direct taxa interactions but could also indicate taxa environmental associations and/or disassociations.

Based on the literature, we can make predictions about how we may expect metacommunity structure to change throughout these Ediacaran assemblages. We predict that the increase in taxonomic and morphological diversity between the Avalon and White Sea assemblages [5] is reflected in more ecological complexity in terms of increased taxa co-occurrences. We predict that the total set of Ediacaran data exhibits strong metacommunity structure that reflects the previously recovered assemblages [7–9] and that the influence of environmental gradients increases between the Avalon and White Sea assemblages [18]. Finally, we will use these analyses to test between 3 hypotheses relating to the underlying causes behind the White Sea–Nama drop in taxonomic diversity: (1) Null hypothesis: Changes in taxonomic diversity are not present or are not detectable; (2) External mass extinction: test whether there is evidence of a catastrophic extinction event between the White Sea and Nama [9,22,46]. Such an event would lead to negative turnover, so a nested metacommunity structure ([40]; or 3) Internal restructuring: increased ecological complexity via co-occurrences and strong metacommunity leading to stronger niche partitioning.

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