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1 Patterns of species range evolution in Indo-Pacific reef assemblages reveal 2 the Coral Triangle as a net source of transoceanic diversity 3 4 Sean M. Evans1, Caroline McKenna1, Stephen D. Simpson2, Jennifer Tournois1,3, 5 Martin J. Genner1 6 7 1 School of Biological Sciences, University of Bristol, Bristol BS8 1TQ. 8 2 Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, 9 EX4 4QD, UK 10 3 Centre for Marine Biodiversity, Exploitation and Conservation, UMR MARBEC (IRD – 11 Ifremer – Univ. Montpellier – CNRS), Université Montpellier 2, Bât 24, Place Eugène 12 Bataillon, 34095 Montpellier Cedex 5, France 13 14 Email: [email protected] 1 15 The Coral Triangle in the Indo-Pacific is a renowned region of exceptional marine 16 biodiversity. The area could be a net source of extant biodiversity, either by acting as a refuge 17 of biodiversity during Pleistocene sea level changes, or as a region where speciation has been 18 prolific. Alternatively, or additionally, the region could be a net sink of biodiversity, where 19 species with origins elsewhere accumulate in the Coral Triangle due its central position in the 20 Indo-Pacific and the availability of suitable habitat. Here we addressed whether the Coral 21 Triangle is a net source or sink of biodiversity by reconstructing species range evolution of 22 45 species (314 populations) of Indo-Pacific reef-associated organisms using a DNA 23 sequence-based coalescent approach. Our results show that populations undergoing the most 24 ancient population establishment were significantly more likely to be closer to the centre of 25 the Coral Triangle than in peripheral locations. The data are consistent with the Coral 26 Triangle being a net source of coral reef biodiversity for the Indo-Pacific region, and they 27 provide a compelling example of how a keystone location can influence the large-scale 28 distributions of biodiversity over evolutionary timescales. 29 30 Keywords: biogeography, coral reef, climate change, species distributions, Bayesian Skyline 31 Plot. 2 32 1. Introduction 33 Understanding the causes of spatial distributions of biodiversity is a fundamental goal of 34 contemporary ecology and evolutionary biology. Global-scale analyses of marine diversity 35 show that some locations are unusually rich in species (1), and knowledge of the underlying 36 causes of such patterns can have implications for conservation and sustainable exploitation in 37 a changing world (2). The Coral Triangle, otherwise known as the Indo-Australian 38 Archipelago, is a region of the Indo-Pacific characterised by coral-rich shelf-seas, and a high 39 diversity of reef-associated organisms (3-5), including over 2000 species of coral-reef- 40 associated fishes (6). From phylogeographic studies of individual taxa in the region, it is clear 41 that many species show strong spatial genetic structuring, suggesting limited adult dispersal 42 and larval retention (7-9). Thus, we can largely reject the concept of panmixia within reef- 43 associated species across the region, and instead we can consider the relative ages of 44 populations within a species. This provides a useful opportunity to investigate whether 45 specific locations have acted as sources or sinks for individual species. 46 47 There is evidence that the Coral Triangle region is a contact zone of taxa for some species 48 that have diversified in allopatry (centre of accumulation/overlap; 10), while other studies 49 suggest that it is the source of extant regional diversity, either being a region of origin of 50 species (11), or a centre of survival (12). In support of the survival hypothesis there is 51 evidence that coral-reef fish species richness on a global scale can be best predicted by 52 proximity to reef refugia during the Pleistocene sea level changes driven by changes in global 53 climate (2). Complementary work using reconstructions of historical biogeography has 54 suggested that the Coral Triangle may have had a changing role through time, where it 55 initially acted as a region of accumulation and survival during the Palaeocene/Eocene, before 56 acting as a centre of origination during the Miocene, and most recently as a centre of survival 3 57 and export during the Pliocene (13). Under this model, the region should have acted as a net 58 source of species for the surrounding Indo-Pacific region. Here we tested this hypothesis 59 explicitly by reconstructing the historic population sizes of reef-associated species and 60 estimating the relative timing of their population establishments. Specifically, we 61 hypothesised that if the Coral Triangle has acted as a source of extant diversity then 62 populations of individual species in closest proximity to the region should have undergone 63 the most ancient population establishments, and there should be an overall reduction in the 64 relative timing of population establishments with increasing distance from the region. 65 66 2. Material and methods 67 68 We sourced published population-level DNA sequence data from Genbank 69 (http://www.ncbi.nlm.nih.gov/genbank/) for broadly-distributed Indo-Pacific reef-associated 70 fish and invertebrates with a partial distribution in the Coral Triangle region. We used data 71 for species that had sequences from three or more locations, where eight or more individuals 72 had been sampled from each, and where at least one of the locations sampled was within 73 2500 km of our approximated centre of the Coral Triangle (approximated as 1°35’ S, 135°20' 74 E, following maps in Green & Mous [4; Fig. 1]). In total this yielded data from 45 species, 75 314 populations in total, and an average of 6.97 (range 3 to 23) populations per species 76 (Electronic Supplementary Material: Table S1). We aligned data for each species separately 77 using ClustalW in DAMBE (14), and reconstructed the effective population size through time 78 for each population separately using Bayesian skyline plots in BEAST version 1.8.2 (15). 79 Each analysis was run for 10 million steps, using the HKY+Γ model. We employed a strict 80 molecular clock, and a coalescence Bayesian skyline tree prior with either the default 10 81 grouped coalescent intervals, or instead 4 groups where 10 or fewer individual sequences 4 82 were available from a location. Operators were set to autooptimise, and parameters were 83 logged every 1000 iterations. All other search parameters were as default. We aimed to 84 generate only information on the relative timing of effective population size changes, so no 85 temporal calibrations were employed. Bayesian skyline plots were plotted using Tracer 1.5 86 (16). All populations showed evidence of a expansion towards the present day. Thus, we 87 were able to identify the point in relative time where there was a pattern of constant 88 population expansion towards the present day (17). We refer to this as the time of population 89 establishment. Occasionally, populations showed declines in population size after a period of 90 population establishment. Here we only use the point of initial population expansion as the 91 time of population establishment. 92 We estimated the distance of each of the 314 sampled populations to the centre of the 93 Coral Triangle (Fig. 1). For each species we fitted a regression line to the relationship 94 between the distance from the centre of the Coral Triangle and the relative time of population 95 establishment. Data for both variables were standardised (mean = 0 and standard deviation = 96 1), ensuring a regression intercept of zero for all species, and enabling the calculation of a 97 standardised slope for each species. These slopes were compared to an expected mean slope 98 of zero using a one-sample t-test, and bias in the direction of slopes was tested using a 99 binomial test. We also tested if populations undergoing the earliest expansions were 100 relatively closer to the centre of the Coral Triangle than those undergoing the latest 101 establishments using a paired t-test. 102 103 3. Results and Discussion 104 105 There was a consistent pattern of the populations undergoing later establishment being closest 106 to the estimated centre of the Coral Triangle (30 of 45 species, binomial test, p = 0.010, Fig 5 107 2a, Electronic Supplementary Material: Table S2). The slope of the relationship between 108 geographic distance from the centre of the Coral Triangle and the relative time of population 109 establishment was significantly negative (one sample t-test, mean slope = -0.215, n = 45, t = - 110 2.51, p = 0.016, Fig 2a). Populations undergoing the earliest establishments were closer to the 111 centre of the Coral Triangle than those undergoing the latest establishments (paired t-test, t = 112 -3.071, p = 0.004, Fig. 2b, Electronic Supplementary Material: Table S2). Together these 113 results support the hypothesis that the Coral Triangle has acted as a net source of extant Indo- 114 Pacific coral reef diversity. 115 116 We assumed that populations that have undergone the most ancient establishments are the 117 most likely source of present genetic diversity while those that have undergone more recent 118 establishments are in sink locations. However, we did not explicitly consider genetic 119 interrelationships of populations. Several issues require consideration. First, the extent of 120 genetic connectivity among populations is dependent on life history (duration of larval 121 pelagic dispersal phase), and habitat specialisation (18,19). Demographic patterns may 122 therefore have become homogenised in some species with extensive dispersal since initial 123 colonisation. Second, phenotypically-similar allopatric populations may have persisted in 124 multiple refugia, in which case population spread following the Pleistocene sea level changes 125 may have been from multiple geographically-segregated sources (20). Third, studies have 126 demonstrated multiple sympatric clades which may represent cryptic species with 127 overlapping distributions (21-22), suggesting that finer scale taxonomic resolution may be 128 required to fully evaluate patterns of population persistence and dispersal. Finally, there is 129 evidence of hybridization among reef-associated species (23), which would make patterns of 130 population establishment difficult to recover. Clearly, therefore, further investigations require 131 accurate dating of the time of population establishments, alongside quantification of the 6 132 direction and timing of reciprocal gene flow, ideally using information from genome-wide 133 markers (24). 134 135 Our results support the concept that refugia have a pivotal role in the recovery of 136 communities following dramatic Pleistocene habitat loss. This emphasises the importance of 137 refugia to preventing biodiversity loss, and has relevance to ongoing threats to shallow water 138 reef communities through habitat destruction, ocean acidification and thermal stress linked to 139 climate change (25). It has been projected that many species of coral will lose habitat over the 140 next century (26), and the incidence of bleaching will become more frequent (27). Long-term 141 conservation of tropical reef biotas in a warming world may therefore depend on the 142 identification and preservation of future potential refugia (28). 143 144 Acknowledgements 145 We are grateful to the many researchers who provided full details of sampling locations of 146 published sequences, either directly on Genbank, or following our requests for further 147 information. 148 149 References 150 1. Tittensor DP, Mora C, Jetz W, Lotze HK, Ricard D, Berghe EV, Worm B. 2010 Global 151 patterns and predictors of marine biodiversity across taxa. Nature 466, 1098-1101. 152 2. Pellissier L, Leprieur F, Parravicini V, Cowman PF, Kulbicki M, Litsios G, Olsen SM, 153 Wisz SM, Bellwood DR, Mouillot D. 2014 Quaternary coral reef refugia preserved fish 154 diversity. Science 344, 1016-1019. 155 156 3. Hughes TP, Bellwood DR, Connolly SR. 2002 Biodiversity hotspots, centres of endemicity, and the conservation of coral reefs. Ecol. Lett. 5, 775-784. 7 157 158 159 160 161 162 4. 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Examples of the use of Bayesian skyline plots to determine relative timing of 224 population establishment: 225 thousand-spot cone (Conus miliaris). Circle diameter indicates relative timing of population 226 establishment. The Coral Triangle ecoregion is highlighted with a dashed line, with the 227 approximate centre indicated with a white square. a) bluestreak cleaner wrasse (Labroides dimidiatus), and b) 228 229 Figure 2. a) Individual species regression lines fitted to relationships between relative 230 distance to centre of Coral Triangle and relative timing of population establishment. Relative 231 times and distances were standardised (mean = 0, SD = 1), enabling an average regression 232 slope to be calculated (shown in black). b) Average geographic distance (±95% confidence 233 intervals) of populations with the earliest and latest population establishment, as estimated 234 from Bayesian skyline plots. 235 11