Phylogeography and marine retention

Authors


Abstract

A number of studies now point to the association of patterns of phylogeography with discontinuities in coastal current patterns. If such phylogeographic patterns are indicative of populations that retain local diversity, as has been predicted by recent modelling, such results may be of use in marine reserve planning. Here we show that there is a distributional correlation on the Pacific coast of North America between marine reserve placement and phylogeographic patterns. A number of factors could contribute to this correlation, but its existence suggests the utility of genetic studies in marine conservation planning.

A recent study in the Journal of Biogeography by Pelc et al. (2009) showed that, for marine species with planktonically dispersing larvae, phylogeographic breaks tend to coaggregate with discontinuities in coastal current patterns. Their result is a timely reminder that contemporary processes should be considered in the maintenance of diversity, perhaps more than the processes from which this diversity originated. A modern solution to the maintenance of extant marine diversity is the establishment of marine protected areas (MPAs). These are designated areas with limits on harvest or gear usage, and have so far been considered a success; regardless of size, reserves protect reproductive populations and have afforded an increase in biomass for study species (Halpern, 2003). A fundamental aim, in addition to identifying regions with high species diversity, is to ensure that these areas promote diversity in neighbouring regions as well (McNeill, 1994; Botsford et al., 2001).

At issue are the demographic connections among populations: which areas act as sources (i.e. areas with a demographic excess; Pulliam, 1988) that subsidize diversity throughout the community? In marine systems, connectivity must usually be inferred indirectly (Thorrold et al., 2002). Recent studies (Galindo et al., 2006) have integrated physical oceanographic models with empirical genetic data from marine species in order better to illuminate the mean patterns of dispersal and recruitment. In a landmark paper, Cowen et al. (2006) generated such an integrative model to describe connectivity among populations of Caribbean reef fish. Their results indicated that significant demographic contributions are often restricted – in part through larval behaviour – to nearby sites, and that currents can influence whether a region is ‘isolated’ from upstream regions; the basin-scale patterns of isolation observed by these authors in the Caribbean correspond to patterns of genetic and morphological clines observed across a range of marine taxa. Such intriguing associations suggest that oceanography is a strong indicator of marine diversity at many levels of organization (Wares et al., 2001; Pelc et al., 2009).

Pringle & Wares (2007) developed a Lagrangian model to describe larval dispersal in advective environments, with the goal of understanding how phylogeographic transitions are maintained. They show that the most important regions in a species’ distribution range, when advection is a dominant factor in dispersal, are those areas with high larval retention – defined as the effect of individual reproduction that is sufficient to overcome the mean and variance of downstream displacement of offspring. Thus, an area exhibiting retention in an advective environment is self-sustaining, despite the general export of offspring to downstream sites. These areas of retention act as population sources, and constitute areas in which novel traits or alleles can be maintained. In regions where reproduction is insufficient to overcome the influence of nearshore currents, any trait that arises among individuals in that region can only be transient (Wares & Pringle, 2008). Thus, characterization of genetic discordance along a current-dominated coast may signify nearby populations with higher retention and production of larvae that supplement downstream populations.

Our own summary of such genetic patterns (see below) is strongly concordant with that of Pelc et al. (2009). Because such patterns are unstable in advective environments unless there is sufficient larval retention, these data – particularly in regions where many such discontinuities overlap – could represent a complementary approach for identifying areas that are important for sustainable fishing and ecosystem function. Finding concordance among phylogeographic histories in a number of species strengthens the inference for a common mechanism that acts broadly on species dynamics (Avise, 2000). We searched for published studies on the Atlantic and Pacific coasts of North America that found a signal for strong genetic differentiation within species, including those studies that reported either a type I phylogeographic break (Avise, 2000) or a minimum FST value of 0.20, as suggested by Wright (1978). Our search as of late 2006 resulted in 25 studies from the Pacific coast, and 16 from the Atlantic coast. Genetic discontinuities were tabulated per 1° latitude, with a latitudinally weighted average used for genetic discontinuities occurring over a wider range (representing either broad clines or spatial sampling error). Again, the results of our survey (see Appendix S1 in Supporting Information) are comparable to the syntheses of Dawson (2001), Wares (2002) and Pelc et al. (2009).

We then summarized information from available MPA databases and resources (e.g. http://www.mpa.gov) including data on location, area, implementation (state or federal) and protection (‘no take’, limited gear use, etc.). Our synthesis was not restricted to ‘no take’ areas, because all levels of coastal protection appear to improve biomass and species diversity (Halpern, 2003). We then analysed the relationship between the latitudinal distribution of phylogeographic discontinuities (weighted number per latitudinal bin) and MPAs (area per latitudinal bin, as well as presence /absence per latitudinal bin) using a nonparametric permutation test (1000 replicates) of Pearson’s correlation, implemented in the PopTools add-in (http://www.cse.csiro.au/poptools) for Microsoft Excel. There was a significant correlation between the location and spatial extent of these features on the Pacific coast (= 0.465, < 0.025; see Fig. 1) but not on the Atlantic coast (= 0.263, < 0.16). This result holds when MPAs are reduced simply to presence/absence per 1° latitude (Pacific = 0.55, < 0.01; Atlantic = 0.17, < 0.20). The inferred breadth of clines on the Atlantic coast (average 4.5° latitude) is twice as wide as those of the Pacific coast (average 2.3°).

Figure 1.

 Histogram indicating relative locations and extent of phylogeographic breaks (number present per latitude, black bars) and log area (km2) of marine protected areas (MPAs; grey bars) along the Pacific coast of North America. Although the topography of the coast could influence the apparent extent of MPAs in a latitudinal bin, the correlation is significant (< 0.01) whether using total area or simply presence / absence.

There are many clear differences between the two coasts in terms of oceanography, taxonomic composition and anthropogenic history (Robinson & Brink, 2004). The poor correlation on the Atlantic coast may be attributed to greater uncertainty in the distribution of phylogeographic patterns (Wares, 2002), or to fewer and less extensive MPAs on this coast. These results may conflate different MPA types, and do not distinguish the variety of life histories (e.g. reproductive biology) among the species considered. Here we include all available observations (as of late 2006) simply because there were limited data (the June 2009 launch of the World Database on Marine Protected Areas, http://www.wdpa-marine.org, dramatically improves access to these data), and subdivision of this information limited statistical testing. It should be emphasized that all MPAs are not equal; for example, those managed as National Marine Sanctuaries do not actually restrict fishing. They have also been established by a variety of agencies and based on various rationales (Brumbaugh et al., 2008).

Although our data suggest a relationship between the biological features that have been considered to identify sites for MPAs and sites that may have greater larval retention and self-recruitment – based at this point solely on reported phylogeographic indicators – it is of course recognized that this is only a correlation. We do not imply the existence of a direct causative relationship between the locations of these varied conservation areas and the summarized phylogeographic patterns, but propose that the correlation merits further exploration. The retention of diversity in these regions – through adequate production, larval behaviour, or other mechanisms – is sufficient to maintain distinct genetic patterns in the face of strong advection, suggesting that the association between genetic clines and the characteristics that have independently been used to develop successful MPAs (e.g. habitat diversity) might not be spurious. Based on the length of time that their larvae spend developing in the water column, most of the species considered here are likely to be strongly influenced by currents. However, even the species with direct development may reflect the environmental gradients to which the planktonic species are responding. Genetic diversity measures have not typically been used in MPA design (Bell & Okamura, 2005) but there is a growing discussion on the utility of such data for this purpose (Gerber et al., 2003; Palumbi et al., 2003). Although biogeographical information has been proposed for the selection of MPAs, it is difficult to identify regions that will truly act as sources of diversity for the species range (Turpie et al., 2000). Patterns of genetic variation may help in the identification of persistent and self-sustaining populations, and may be critical for the management of fisheries (Swain et al., 2007).

Another concern with marine reserve placement is that climate change may significantly redistribute species, patterns of productivity, and interactions. In recent decades, sea surface temperatures have changed considerably, and subsequent shifts in marine species distributions are well documented (Southward, 1991; Barry et al., 1995; Walther et al., 2002; Perry et al., 2005; Helmuth et al., 2006; Portner & Knust, 2007). The monitoring of MPAs may be necessary to clarify whether the conditions that were considered when the areas were established are changing. Genetic clines can be objectively monitored over time (Burton, 1997; Rose et al., 2006; Hoffmann & Daborn, 2007), which may permit more flexibility in establishing and maintaining marine reserves.

Phylogeographic patterns cannot replace other empirical and modelling studies that evaluate the diversity, productivity and suitability of a site for the placement of a marine reserve. However, if we recognize that such transition regions are more likely to represent areas of strong environmental transition and populations with high fitness in that portion of the coastal environment, then phylogeographic studies can be viewed as more than windows onto the past – they can be understood as indicators of contemporary processes that may be important for the maintenance of coastal diversity. Still, it is important to recognize that our results are based on a small number of genetic studies, most of which are in need of an update through additional geographical or genomic sampling. It would be premature to base current marine reserve design efforts on a small number of genetic data. However, to date very few studies have explicitly looked for the potentially subtle results that could match our hypothesis well. For example, highly asymmetric gene flow may have a significant evolutionary signal that cannot be illuminated with traditional phylogeographic approaches (Wares et al., 2001). As more directed genetic studies evaluate the potential for asymmetric restrictions on gene flow, there will be more information for marine reserve design efforts.

Syntheses such as that by Pelc et al. (2009) emphasize that ongoing, contemporary processes are responsible for maintaining patterns of intraspecific diversity. Other studies show that oceanographic phenomena that drive diversity patterns in single species are likely to influence entire marine communities (Barber et al., 2000; Wares et al., 2001; Genin et al., 2005). The identification of regional source populations must be a high priority in marine management, because the loss of source habitat and populations may have cascade effects on surrounding marine – and human – communities. It is clear that there should be some relationship between our efforts to preserve biodiversity and the natural processes that promote it (Bowen, 1999). Although we are cautious in interpreting the correlative results shown above, they suggest future avenues of research towards understanding how oceanographic forces influence productivity, phylogeography and biogeography.

Acknowledgements

Thanks to Jamie Pringle, Robin Pelc and an anonymous referee for their extremely helpful insights during the preparation of this manuscript.

Editor: David Bellwood

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