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Understanding the evolutionary processes that have shaped existing patterns of genetic diversity of reef-building corals over broad scales is required to inform long-term conservation planning. Genetic structure and diversity of the mass-spawning hard coral, Acropora tenuis, were assessed with seven DNA microsatellite loci from a series of isolated and discontinuous coastal and offshore reef systems in northwest Australia. Significant subdivision was detected among all sites (FST = 0.062, RST = 0.090), with the majority of this variation due to genetic differentiation among reef systems. In addition, genetic divergence was detected between the coastal and offshore zones that cannot be adequately explained by geographic distance, indicating that transport of larvae between these zones via large-scale oceanic currents is rare even over time frames that account for connectivity over multiple generations. Significant differences in the amount of genetic diversity at each system were also detected, with higher diversity observed on the lower latitude reefs. The implications are that these reef systems of northwest Australia are not only demographically independent, but that they will also have to rely on their own genetic diversity to adapt to environmental change over the next few decades to centuries.
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- Materials and methods
- Literature cited
- Supporting Information
Coral reefs around the world are being degraded by an increasing range of disturbances which operate over various spatial and temporal scales (Nyström et al. 2000; Pandolfi et al. 2003). The ability of coral reefs to not only recover from, but also to adapt to, altered disturbance regimes is highly dependent upon the pattern and strength of connections among populations via dispersal of larvae – the mechanisms and consequences of which also vary in space and time. Contemporary dispersal of large numbers of larvae is important for the demographic recovery and persistence of populations and often operates over local scales (Gaines et al. 2007). Conversely, because geographic isolation among populations will eventually lead to unique genetic lineages, weaker historical connections are important for evolutionary processes affecting species distributions, genetic diversification, and adaptation (Fraser and Bernatchez 2001; Moritz 2002; Bowen and Roman 2005). Therefore, to mitigate the impacts of different disturbances on coral systems, an understanding of the multiple temporal and spatial scales of connectivity is required to inform appropriate management strategies (Kinlan et al. 2005; Cowen et al. 2007).
In the far northwest of Australia (NWA), recent genetic work on corals has focused on elucidating patterns of local-scale dispersal that primarily influence short-term persistence of populations (e.g. Whitaker 2004; Underwood et al. 2007, 2009), but consideration also needs to be given to how corals will respond to climate change and other anthropogenic impacts over the next few decades to centuries. This longer-term conservation planning requires an investigation of the evolutionary processes that have shaped the distribution of genetic diversity of coral reefs over broad scales (van Oppen and Gates 2006; Rocha et al. 2007).
Within the region of NWA, corals form discontinuous reef systems that are either coastal reefs adjacent to the mainland, or are isolated offshore reefs located along the margin of the continental shelf in the Timor Sea (Fig. 1). The continental shelf is more than 100 km wide north and east of Ningaloo Reef, and presumably small changes in sea-level would have altered the distribution of coral reefs that fringed this section of the mainland. For example, at low sea levels during the last glacial period (from about 110–18 000 years ago), most of the continental shelf was exposed, and any fringing coral reefs would have been much closer to the offshore reefs. However, there is currently no evidence pertaining to the existence of such fringing reefs, but offshore reefs probably existed during the late Tertiary–Quaternary (Collins 2002). In addition to sea level variation, changes in oceanic circulation and temperature undoubtedly influenced the distribution of coral reef species (Wyrwoll et al. in press). Therefore, while large changes in geographic position of fringing reefs must have occurred in recent geological history, it is not obvious whether the offshore reefs may also have come and gone, or whether genetic connections between the offshore and coastal zones were maintained during these changes.
Figure 1. Map of northern Western Australia, showing the bathymetry of the continental shelf and the coastal and offshore coral reefs where genetic samples of A. tenuis were collected.
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Until recently, it has been assumed that the offshore systems of NWA and the coastal systems further south and west are strongly connected by a poleward flowing current which originates in the Indonesian Throughflow and moves through the Timor Sea along the continental shelf margin (e.g. Veron 1995; Nof et al. 2002). This flow is strongest in autumn (April/May) (Holloway and Nye 1985; Holloway 1995), during the time of the major mass-spawning of corals and was thought to create unidirectional gene flow between the regionally separated coral reef systems (Simpson 1991). However, in the Timor Sea, this south westerly flow is broad and weak relative to the Leeuwin Current further south (Holloway 1995), and seasonal south-west winds induce a reversal of the current to the north-east in Spring (October/November) (Cresswell et al. 1993). Furthermore, recent oceanographic studies have not been able to identify a direct connection between these water masses and the Leeuwin Current which begins in earnest near the Ningaloo Reef coast at 22°S (Domingues et al. 2007; D'Adamo et al. in press).
Biogeographic evidence also indicates that connectivity between the coastal and offshore zones may be limited. Qualitative differences in species composition between these zones have been observed not only for scleractinian corals, but also for many marine floral and faunal species (B. Wilson, personal communication). Additionally, there is also a quantitative relationship of latitude with the distribution of scleractinian species, whereby species richness declines in systems that are further south (Veron 1995); this may be due to a lack of connectivity or to changes in habitat suitability for non-generalist species.
Patterns of genetic diversity within a species that occurs throughout this region would provide insights into the degree of historical connections between coastal and offshore reefs, systems and zones of NWA; large differences in genetic structure and diversity in abundant populations (i.e. large effective population sizes) from the offshore and coastal systems or zones would suggest that the long-term isolation has been an important influence on biodiversity in this region. Underwood et al. (2009) explored connectivity in the mass-spawning coral Acropora tenuis and the brooding coral Seriatopora hystrix within and between the two offshore systems of Scott Reef and Rowley Shoals, and showed that ecologically relevant gene flow is restricted between systems, between reefs within each system, and even within some reefs. However, while differences between the two systems were significant, the level of this differentiation for the mass-spawner was only moderate (FST = 0.034), suggesting that they are connected by rare dispersal events. Further research is required to assess whether the coastal systems in NWA are differentiated by similar levels.
In this study, I addressed the hypothesis that populations of a reef-building coral species with planktonic dispersal are panmictic in the NWA region. To this end, the distribution of genetic variation of microsatellite DNA markers in the mass-spawning coral Acropora tenuis (Dana) was measured to infer patterns of connectivity among reef systems in the offshore (Scott Reef and Rowley Shoals) and coastal (Dampier Archipelago and Ningaloo Reef) zones of NWA. The Dampier Archipelago is separated from the Rowley Shoals by a similar distance (∼400 km) as Rowley Shoals is from Scott Reef (Fig. 1). Ningaloo Reef is the other major coastal system of coral reefs in NWA, and the northern tip of this system is located about 300 km south-west of the Dampier Archipelago (Fig. 1). Thus, these two coastal systems provide an excellent opportunity to test whether genetic differences between the offshore and coastal zones are greater than differences within the two zones, unconfounded by the extent of geographic separation. Additionally, to gain further insight into degree of isolation, effective population size and the importance of asexual versus sexual reproduction, I test whether genetic and genotypic (clonal) diversities vary between the high-latitude, offshore reefs and the low latitude, coastal reefs.