Genetic Structure of the Caribbean Giant Barrel Sponge Xestospongia Muta Using the I3-M11 Partition of COI
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Coral Reefs DOI 10.1007/s00338-008-0430-3 REPORT Genetic structure of the Caribbean giant barrel sponge Xestospongia muta using the I3-M11 partition of COI S. López-Legentil · J. R. Pawlik Received: 28 March 2008 / Accepted: 7 September 2008 © Springer-Verlag 2008 Abstract In recent years, reports of sponge bleaching, genetic diVerentiation was not due to isolation by distance. disease, and subsequent mortality have increased alarm- While limited larval dispersal may have led to diVerentia- ingly. Population recovery may depend strongly on coloni- tion among some of the populations, the patterns of genetic zation capabilities of the aVected species. The giant barrel structure appear to be most strongly related to patterns of sponge Xestospongia muta is a dominant reef constituent in ocean currents. Therefore, hydrological features may play a the Caribbean. However, little is known about its popula- major role in sponge colonization and need to be consi- tion structure and gene Xow. The 5Ј-end fragment of the dered in future plans for management and conservation of mitochondrial gene cytochrome oxidase subunit I is often these important components of coral reef ecosystems. used to address these kinds of questions, but it presents very low intraspeciWc nucleotide variability in sponges. In Keywords Sponge · Xestospongia muta · Population this study, the usefulness of the I3-M11 partition of COI to genetics · Genetic structure · mtDNA · Ocean currents determine the genetic structure of X. muta was tested for seven populations from Florida, the Bahamas and Belize. A total of 116 sequences of 544 bp were obtained for the I3- Introduction M11 partition corresponding to four haplotypes. In order to make a comparison with the 5Ј-end partition, 10 sequences Sponges are a prominent component of Caribbean coral per haplotype were analyzed for this fragment. The 40 reefs (Diaz and Rützler 2001). In terms of species richness, resulting sequences were of 569 bp and corresponded to abundance, and biomass, sponges rival both hard and soft two haplotypes. The nucleotide diversity of the I3-M11 par- corals (Targett and Schmahl 1984; Diaz and Rützler 2001). tition ( = 0.00386) was higher than that of the 5Ј-end par- In addition, sponges provide refuge for many small inverte- tition ( = 0.00058), indicating better resolution at the brates, are critical to benthic-pelagic coupling, have symbi- intraspeciWc level. Sponges with the most divergent exter- otic associations with microorganisms (Diaz and Rützler nal morphologies (smooth vs. digitate surface) had diVerent 2001), and produce secondary metabolites with interesting haplotypes, while those with the most common external ecological and pharmaceutical properties (reviewed in Paul morphology (rough surface) presented a mixture of haplo- and Ritson-Williams 2008). Sponge larvae can disperse types. Pairwise tests for genetic diVerentiation among geo- over short (e.g., Uriz 1982; Uriz et al. 1998; Mariani et al. W graphic locations based on FST values showed signi cant 2000) or long distances (e.g., Maldonado and Uriz 1999; genetic divergence between most populations, but this Vacelet 1999; Lazoski et al. 2001), depending on the spe- cies. Gene Xow is often correlated with larval dispersal Communicated by Biology Editor Dr Ruth Gates capabilities and population structure, yet the existing molecular studies of sponges have mainly focused on S. López-Legentil (&) · J. R. Pawlik resolving the taxonomically problematic groups (reviewed Center for Marine Science, University of North Carolina Wilmington, 5600 Marvin K. Moss Lane, Wilmington, in Knowlton 2000). NC 28409, USA Although the ecological importance of sponges is well e-mail: [email protected] established, there have been few studies of the genetic 123 Coral Reefs variation among sponge populations and spatial patterns of exceeds that of any other benthic invertebrate. Individuals this variation due to a lack of variable single-copy markers are often very large, with heights and diameters in excess of with enough resolution to diVerentiate populations (Wörhe- 1 m, and some of these large individuals are estimated to be ide et al. 2004, 2005). Microsatellite loci are currently >1,000 years old (McMurray et al. 2008). Individuals of available for only three sponge species (Duran et al. 2002; X. muta are highly variable in size, shape, and external sur- Knowlton et al. 2003; Blanquer et al. 2005), and other face morphology, with the last of these varying from nuclear markers present low nucleotide variability even at smooth to highly digitate or lamellate (Kerr and Kelly- the species level (Blanquer and Uriz 2007) or present Borges 1994). Past studies of the sterol composition of the intragenomic variation that makes them unsuitable for anal- tissues of X. muta have established that distinct chemotypes yses at the population level (nrDNA ITS region; Duran exist (Fromont et al. 1994), but they did not correlate with et al. 2004a; Nichols and Barnes 2005). Recently, the sec- geographic locality, depth, microhabitat, or morphotype ond intron of the nuclear ATP synthetase beta subunit gene (Kerr and Kelly-Borges 1994). (ATPSbeta-iII) has been used to study the population struc- Tissues of X. muta contain cyanobacterial symbionts ture in the two sponges: Pericharax heteroraphis and Leuc- belonging to the Synechococcus group (Gómez et al. 2002; etta chagosensis (Bentlage and Wörheide 2007; Wörheide Steindler et al. 2005). Like reef-building corals, X. muta is et al. 2008). Although these results were promising and subject to occasional bleaching (loss of the reddish-brown showed an increased intraspeciWc diversity when compared coloration; Vicente 1990). Two types of bleaching have to other genetic markers, some potential limitations, includ- been described: cyclic bleaching, from which sponges ing false heterozygotes, the large eVective population size recover, and fatal bleaching, which often results in sponge of bi-allelic nuclear DNA, and potential intragenic recom- death (Cowart et al. 2006). Reports of sponge bleaching binations, need to be considered (Moore 1995; Posada and and disease have increased dramatically in recent years and Crandall 2002; Nichols and Barnes 2005; Bentlage and have been observed throughout the Caribbean (reviewed in Wörheide 2007). Webster 2007). In a recent study of stress proteins in Mitochondrial genes remain the preferred choice for pop- X. muta, López-Legentil et al. (2008) concluded that, as ulation genetic and phylogeographic studies of marine amply demonstrated for corals, an increase in seawater tem- organisms because they are maternally inherited without perature may result in a decline of X. muta populations in recombination, have shorter coalescence times, and are the Caribbean. In addition, elevated seawater temperatures expected to undergo lineage sorting three times faster than may aVect the frequency and severity of disease outbreaks nuclear markers (Avise et al. 1987; Palumbi et al. 2001). by increasing the prevalence and virulence of pathogens, However, few studies have attempted to determine the facilitating new invasions or reducing host resistance and genetic structure of sponge populations using mitochondrial resilience (Sutherland et al. 2004). Therefore, sponge popu- markers (Duran et al. 2004b; Wörheide 2006; Duran and lations are threatened by both global warming and disease. Rützler 2006), and these studies targeted a fragment of the In order to assess the sponge population vulnerability, it is cytochrome c oxidase subunit I (COI) gene ampliWed with important to understand how populations are connected and the universal primers of Folmer et al. (1994; hereafter called to determine their genetic diversity. Knowledge of marine as 5Ј-end partition). The results of these previous studies population connectivity and larval dispersal is critical to revealed low levels of genetic variation between popula- understand past impacts and future prospects for conserva- tions, including those separated by distances of more than tion, and to design appropriate management plans for coral 7,000 km (Duran et al. 2004b; Wörheide 2006). In a recent reef ecosystem biodiversity (Jones et al. 2007). study, Erpenbeck et al. (2006) found that the COI I3-M11 In this study, the variation of the I3-M11 partition of the partition in sponges presented more variability than the mitochondrial COI gene was analyzed for 116 individuals 5Ј-end partition at the species level and, therefore, seemed to from seven populations to determine the genetic structure be more suitable for taxonomic studies and DNA bar-cod- of X. muta in Florida, the Bahamas, and Belize. These spec- ing. To date, however, no study has attempted to determine imens presented the typical vase-shaped morphology with a the usefulness of the I3-M11 partition as a genetic marker to highly irregular surface. In addition, to further test the use- assess the population genetic structure of sponges. fulness of the I3-M11 partition at lower taxonomic levels, The giant barrel sponge, Xestospongia muta (Demo- 10 specimens of each haplotype detected with the I3-M11 spongiae: Haplosclerida) is a large and common member of partition were sequenced for the 5Ј-end partition using Fol- Caribbean coral reef communities. Populations of this spe- mer et al. (1994) universal primers. Finally, eight speci- cies occupy greater than 9% of the available reef substrate mens presenting the most divergent morphologies (four in some regions (Zea 1993). On the reefs oV Key Largo,