Download The Coral Triangle as a net source of Indo

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Patterns of species range evolution in Indo-Pacific reef assemblages reveal
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the Coral Triangle as a net source of transoceanic diversity
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Sean M. Evans1, Caroline McKenna1, Stephen D. Simpson2, Jennifer Tournois1,3,
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Martin J. Genner1
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1 School of Biological Sciences, University of Bristol, Bristol BS8 1TQ.
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2 Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter,
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EX4 4QD, UK
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3 Centre for Marine Biodiversity, Exploitation and Conservation, UMR MARBEC (IRD –
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Ifremer – Univ. Montpellier – CNRS), Université Montpellier 2, Bât 24, Place Eugène
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Bataillon, 34095 Montpellier Cedex 5, France
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Email: [email protected]
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The Coral Triangle in the Indo-Pacific is a renowned region of exceptional marine
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biodiversity. The area could be a net source of extant biodiversity, either by acting as a refuge
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of biodiversity during Pleistocene sea level changes, or as a region where speciation has been
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prolific. Alternatively, or additionally, the region could be a net sink of biodiversity, where
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species with origins elsewhere accumulate in the Coral Triangle due its central position in the
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Indo-Pacific and the availability of suitable habitat. Here we addressed whether the Coral
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Triangle is a net source or sink of biodiversity by reconstructing species range evolution of
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45 species (314 populations) of Indo-Pacific reef-associated organisms using a DNA
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sequence-based coalescent approach. Our results show that populations undergoing the most
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ancient population establishment were significantly more likely to be closer to the centre of
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the Coral Triangle than in peripheral locations. The data are consistent with the Coral
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Triangle being a net source of coral reef biodiversity for the Indo-Pacific region, and they
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provide a compelling example of how a keystone location can influence the large-scale
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distributions of biodiversity over evolutionary timescales.
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Keywords: biogeography, coral reef, climate change, species distributions, Bayesian Skyline
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Plot.
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1. Introduction
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Understanding the causes of spatial distributions of biodiversity is a fundamental goal of
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contemporary ecology and evolutionary biology. Global-scale analyses of marine diversity
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show that some locations are unusually rich in species (1), and knowledge of the underlying
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causes of such patterns can have implications for conservation and sustainable exploitation in
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a changing world (2). The Coral Triangle, otherwise known as the Indo-Australian
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Archipelago, is a region of the Indo-Pacific characterised by coral-rich shelf-seas, and a high
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diversity of reef-associated organisms (3-5), including over 2000 species of coral-reef-
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associated fishes (6). From phylogeographic studies of individual taxa in the region, it is clear
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that many species show strong spatial genetic structuring, suggesting limited adult dispersal
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and larval retention (7-9). Thus, we can largely reject the concept of panmixia within reef-
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associated species across the region, and instead we can consider the relative ages of
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populations within a species. This provides a useful opportunity to investigate whether
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specific locations have acted as sources or sinks for individual species.
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There is evidence that the Coral Triangle region is a contact zone of taxa for some species
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that have diversified in allopatry (centre of accumulation/overlap; 10), while other studies
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suggest that it is the source of extant regional diversity, either being a region of origin of
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species (11), or a centre of survival (12). In support of the survival hypothesis there is
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evidence that coral-reef fish species richness on a global scale can be best predicted by
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proximity to reef refugia during the Pleistocene sea level changes driven by changes in global
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climate (2). Complementary work using reconstructions of historical biogeography has
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suggested that the Coral Triangle may have had a changing role through time, where it
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initially acted as a region of accumulation and survival during the Palaeocene/Eocene, before
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acting as a centre of origination during the Miocene, and most recently as a centre of survival
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and export during the Pliocene (13). Under this model, the region should have acted as a net
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source of species for the surrounding Indo-Pacific region. Here we tested this hypothesis
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explicitly by reconstructing the historic population sizes of reef-associated species and
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estimating the relative timing of their population establishments. Specifically, we
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hypothesised that if the Coral Triangle has acted as a source of extant diversity then
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populations of individual species in closest proximity to the region should have undergone
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the most ancient population establishments, and there should be an overall reduction in the
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relative timing of population establishments with increasing distance from the region.
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2. Material and methods
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We
sourced
published
population-level
DNA
sequence
data
from
Genbank
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(http://www.ncbi.nlm.nih.gov/genbank/) for broadly-distributed Indo-Pacific reef-associated
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fish and invertebrates with a partial distribution in the Coral Triangle region. We used data
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for species that had sequences from three or more locations, where eight or more individuals
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had been sampled from each, and where at least one of the locations sampled was within
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2500 km of our approximated centre of the Coral Triangle (approximated as 1°35’ S, 135°20'
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E, following maps in Green & Mous [4; Fig. 1]). In total this yielded data from 45 species,
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314 populations in total, and an average of 6.97 (range 3 to 23) populations per species
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(Electronic Supplementary Material: Table S1). We aligned data for each species separately
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using ClustalW in DAMBE (14), and reconstructed the effective population size through time
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for each population separately using Bayesian skyline plots in BEAST version 1.8.2 (15).
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Each analysis was run for 10 million steps, using the HKY+Γ model. We employed a strict
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molecular clock, and a coalescence Bayesian skyline tree prior with either the default 10
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grouped coalescent intervals, or instead 4 groups where 10 or fewer individual sequences
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were available from a location. Operators were set to autooptimise, and parameters were
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logged every 1000 iterations. All other search parameters were as default. We aimed to
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generate only information on the relative timing of effective population size changes, so no
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temporal calibrations were employed. Bayesian skyline plots were plotted using Tracer 1.5
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(16). All populations showed evidence of a expansion towards the present day. Thus, we
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were able to identify the point in relative time where there was a pattern of constant
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population expansion towards the present day (17). We refer to this as the time of population
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establishment. Occasionally, populations showed declines in population size after a period of
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population establishment. Here we only use the point of initial population expansion as the
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time of population establishment.
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We estimated the distance of each of the 314 sampled populations to the centre of the
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Coral Triangle (Fig. 1). For each species we fitted a regression line to the relationship
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between the distance from the centre of the Coral Triangle and the relative time of population
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establishment. Data for both variables were standardised (mean = 0 and standard deviation =
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1), ensuring a regression intercept of zero for all species, and enabling the calculation of a
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standardised slope for each species. These slopes were compared to an expected mean slope
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of zero using a one-sample t-test, and bias in the direction of slopes was tested using a
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binomial test. We also tested if populations undergoing the earliest expansions were
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relatively closer to the centre of the Coral Triangle than those undergoing the latest
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establishments using a paired t-test.
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3. Results and Discussion
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There was a consistent pattern of the populations undergoing later establishment being closest
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to the estimated centre of the Coral Triangle (30 of 45 species, binomial test, p = 0.010, Fig
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2a, Electronic Supplementary Material: Table S2). The slope of the relationship between
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geographic distance from the centre of the Coral Triangle and the relative time of population
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establishment was significantly negative (one sample t-test, mean slope = -0.215, n = 45, t = -
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2.51, p = 0.016, Fig 2a). Populations undergoing the earliest establishments were closer to the
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centre of the Coral Triangle than those undergoing the latest establishments (paired t-test, t =
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-3.071, p = 0.004, Fig. 2b, Electronic Supplementary Material: Table S2). Together these
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results support the hypothesis that the Coral Triangle has acted as a net source of extant Indo-
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Pacific coral reef diversity.
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We assumed that populations that have undergone the most ancient establishments are the
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most likely source of present genetic diversity while those that have undergone more recent
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establishments are in sink locations. However, we did not explicitly consider genetic
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interrelationships of populations. Several issues require consideration. First, the extent of
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genetic connectivity among populations is dependent on life history (duration of larval
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pelagic dispersal phase), and habitat specialisation (18,19). Demographic patterns may
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therefore have become homogenised in some species with extensive dispersal since initial
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colonisation. Second, phenotypically-similar allopatric populations may have persisted in
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multiple refugia, in which case population spread following the Pleistocene sea level changes
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may have been from multiple geographically-segregated sources (20). Third, studies have
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demonstrated multiple sympatric clades which may represent cryptic species with
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overlapping distributions (21-22), suggesting that finer scale taxonomic resolution may be
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required to fully evaluate patterns of population persistence and dispersal. Finally, there is
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evidence of hybridization among reef-associated species (23), which would make patterns of
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population establishment difficult to recover. Clearly, therefore, further investigations require
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accurate dating of the time of population establishments, alongside quantification of the
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direction and timing of reciprocal gene flow, ideally using information from genome-wide
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markers (24).
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Our results support the concept that refugia have a pivotal role in the recovery of
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communities following dramatic Pleistocene habitat loss. This emphasises the importance of
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refugia to preventing biodiversity loss, and has relevance to ongoing threats to shallow water
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reef communities through habitat destruction, ocean acidification and thermal stress linked to
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climate change (25). It has been projected that many species of coral will lose habitat over the
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next century (26), and the incidence of bleaching will become more frequent (27). Long-term
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conservation of tropical reef biotas in a warming world may therefore depend on the
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identification and preservation of future potential refugia (28).
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Acknowledgements
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We are grateful to the many researchers who provided full details of sampling locations of
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published sequences, either directly on Genbank, or following our requests for further
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information.
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Figure Legends
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Figure 1. Examples of the use of Bayesian skyline plots to determine relative timing of
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population establishment:
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thousand-spot cone (Conus miliaris). Circle diameter indicates relative timing of population
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establishment. The Coral Triangle ecoregion is highlighted with a dashed line, with the
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approximate centre indicated with a white square.
a) bluestreak cleaner wrasse (Labroides dimidiatus), and b)
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Figure 2. a) Individual species regression lines fitted to relationships between relative
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distance to centre of Coral Triangle and relative timing of population establishment. Relative
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times and distances were standardised (mean = 0, SD = 1), enabling an average regression
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slope to be calculated (shown in black). b) Average geographic distance (±95% confidence
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intervals) of populations with the earliest and latest population establishment, as estimated
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from Bayesian skyline plots.
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