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Deep genetic divergences among Indo-Pacific populations of the coral reef sponge Leucetta chagosensis (Leucettidae): founder effects, vicariance, or both?

Wörheide G, Epp LS, Macis L - BMC Evol. Biol. (2008)

Bottom Line: Populations along the South Equatorial Current in the south-western Pacific showed isolation-by-distance effects.Overall, the results pointed towards stepping-stone dispersal with some putative long-distance exchange, consistent with expectations from low dispersal capabilities.This structure was perpetuated largely as a result of the life history of L. chagosensis, resulting in high levels of regional isolation.

View Article: PubMed Central - HTML - PubMed

Affiliation: Courant Research Center Geobiology, Georg-August-Universität Göttingen, Goldschmidtstr. 3, D-37077 Göttingen, Germany. gert.woerheide@geo.uni-goettingen.de

ABSTRACT

Background: An increasing number of studies demonstrate that genetic differentiation and speciation in the sea occur over much smaller spatial scales than previously appreciated given the wide distribution range of many morphologically defined coral reef invertebrate species and the presumed dispersal-enhancing qualities of ocean currents. However, knowledge about the processes that lead to population divergence and speciation is often lacking despite being essential for the understanding, conservation, and management of marine biodiversity. Sponges, a highly diverse, ecologically and economically important reef-invertebrate taxon, exhibit spatial trends in the Indo-West Pacific that are not universally reflected in other marine phyla. So far, however, processes generating those unexpected patterns are not understood.

Results: We unraveled the phylogeographic structure of the widespread Indo-Pacific coral reef sponge Leucetta chagosensis across its known geographic range using two nuclear markers: the rDNA internal transcribed spacers (ITS 1&2) and a fragment of the 28S gene, as well as the second intron of the ATP synthetase beta subunit-gene (ATPSb-iII). This enabled the detection of several deeply divergent clades congruent over both loci, one containing specimens from the Indian Ocean (Red Sea and Maldives), another one from the Philippines, and two other large and substructured NW Pacific and SW Pacific clades with an area of overlap in the Great Barrier Reef/Coral Sea. Reciprocally monophyletic populations were observed from the Philippines, Red Sea, Maldives, Japan, Samoa, and Polynesia, demonstrating long-standing isolation. Populations along the South Equatorial Current in the south-western Pacific showed isolation-by-distance effects. Overall, the results pointed towards stepping-stone dispersal with some putative long-distance exchange, consistent with expectations from low dispersal capabilities.

Conclusion: We argue that both founder and vicariance events during the late Pliocene and Pleistocene were responsible to varying degrees for generating the deep phylogeographic structure. This structure was perpetuated largely as a result of the life history of L. chagosensis, resulting in high levels of regional isolation. Reciprocally monophyletic populations constitute putative sibling (cryptic) species, while population para- and polyphyly may indicate incipient speciation processes. The genetic diversity and biodiversity of tropical Indo-Pacific sponges appears to be substantially underestimated since the high level of genetic divergence is not necessarily manifested at the morphological level.

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Leucetta chagosensis in its natural habitat. Leucetta chagosensis in its natural habitat at Ribbon Reef #10, Great Barrier Reef, February 2006. Left: A small specimen with one central osculum. Right: An individual producing asexual buds separating from the main animal. The size of both specimens is approximately 4 cm.
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Figure 6: Leucetta chagosensis in its natural habitat. Leucetta chagosensis in its natural habitat at Ribbon Reef #10, Great Barrier Reef, February 2006. Left: A small specimen with one central osculum. Right: An individual producing asexual buds separating from the main animal. The size of both specimens is approximately 4 cm.

Mentions: Results from the present study suggest that the colonization of new distant habitats by L. chagosensis and the genetic cohesiveness among them cannot be sustained by the dispersal of sexual propagules alone. Occasional long-distance dispersal, either by asexual fragments [32,33] or by rafting [34] might play a role. To date, there is no direct evidence for long-range dispersal in the studied taxon, but the discovery of a budding specimen of L. chagosensis (Fig. 6; G. Wörheide pers. obs. at Ribbon Reef No. 10 in February 2006) provides evidence that asexual dispersal does occur naturally. Such asexual fragments (buds) constitute fully functional mini-sponges that are probably capable of surviving for a considerable amount of time in the plankton (or rafting on pumice, for example) before potentially colonizing distant reef habitats.


Deep genetic divergences among Indo-Pacific populations of the coral reef sponge Leucetta chagosensis (Leucettidae): founder effects, vicariance, or both?

Wörheide G, Epp LS, Macis L - BMC Evol. Biol. (2008)

Leucetta chagosensis in its natural habitat. Leucetta chagosensis in its natural habitat at Ribbon Reef #10, Great Barrier Reef, February 2006. Left: A small specimen with one central osculum. Right: An individual producing asexual buds separating from the main animal. The size of both specimens is approximately 4 cm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2267160&req=5

Figure 6: Leucetta chagosensis in its natural habitat. Leucetta chagosensis in its natural habitat at Ribbon Reef #10, Great Barrier Reef, February 2006. Left: A small specimen with one central osculum. Right: An individual producing asexual buds separating from the main animal. The size of both specimens is approximately 4 cm.
Mentions: Results from the present study suggest that the colonization of new distant habitats by L. chagosensis and the genetic cohesiveness among them cannot be sustained by the dispersal of sexual propagules alone. Occasional long-distance dispersal, either by asexual fragments [32,33] or by rafting [34] might play a role. To date, there is no direct evidence for long-range dispersal in the studied taxon, but the discovery of a budding specimen of L. chagosensis (Fig. 6; G. Wörheide pers. obs. at Ribbon Reef No. 10 in February 2006) provides evidence that asexual dispersal does occur naturally. Such asexual fragments (buds) constitute fully functional mini-sponges that are probably capable of surviving for a considerable amount of time in the plankton (or rafting on pumice, for example) before potentially colonizing distant reef habitats.

Bottom Line: Populations along the South Equatorial Current in the south-western Pacific showed isolation-by-distance effects.Overall, the results pointed towards stepping-stone dispersal with some putative long-distance exchange, consistent with expectations from low dispersal capabilities.This structure was perpetuated largely as a result of the life history of L. chagosensis, resulting in high levels of regional isolation.

View Article: PubMed Central - HTML - PubMed

Affiliation: Courant Research Center Geobiology, Georg-August-Universität Göttingen, Goldschmidtstr. 3, D-37077 Göttingen, Germany. gert.woerheide@geo.uni-goettingen.de

ABSTRACT

Background: An increasing number of studies demonstrate that genetic differentiation and speciation in the sea occur over much smaller spatial scales than previously appreciated given the wide distribution range of many morphologically defined coral reef invertebrate species and the presumed dispersal-enhancing qualities of ocean currents. However, knowledge about the processes that lead to population divergence and speciation is often lacking despite being essential for the understanding, conservation, and management of marine biodiversity. Sponges, a highly diverse, ecologically and economically important reef-invertebrate taxon, exhibit spatial trends in the Indo-West Pacific that are not universally reflected in other marine phyla. So far, however, processes generating those unexpected patterns are not understood.

Results: We unraveled the phylogeographic structure of the widespread Indo-Pacific coral reef sponge Leucetta chagosensis across its known geographic range using two nuclear markers: the rDNA internal transcribed spacers (ITS 1&2) and a fragment of the 28S gene, as well as the second intron of the ATP synthetase beta subunit-gene (ATPSb-iII). This enabled the detection of several deeply divergent clades congruent over both loci, one containing specimens from the Indian Ocean (Red Sea and Maldives), another one from the Philippines, and two other large and substructured NW Pacific and SW Pacific clades with an area of overlap in the Great Barrier Reef/Coral Sea. Reciprocally monophyletic populations were observed from the Philippines, Red Sea, Maldives, Japan, Samoa, and Polynesia, demonstrating long-standing isolation. Populations along the South Equatorial Current in the south-western Pacific showed isolation-by-distance effects. Overall, the results pointed towards stepping-stone dispersal with some putative long-distance exchange, consistent with expectations from low dispersal capabilities.

Conclusion: We argue that both founder and vicariance events during the late Pliocene and Pleistocene were responsible to varying degrees for generating the deep phylogeographic structure. This structure was perpetuated largely as a result of the life history of L. chagosensis, resulting in high levels of regional isolation. Reciprocally monophyletic populations constitute putative sibling (cryptic) species, while population para- and polyphyly may indicate incipient speciation processes. The genetic diversity and biodiversity of tropical Indo-Pacific sponges appears to be substantially underestimated since the high level of genetic divergence is not necessarily manifested at the morphological level.

Show MeSH
Related in: MedlinePlus