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Oceanic dispersal barriers, adaptation and larval retention: an interdisciplinary assessment of potential factors maintaining a phylogeographic break between sister lineages of an African prawn.

Teske PR, Papadopoulos I, Newman BK, Dworschak PC, McQuaid CD, Barker NP - BMC Evol. Biol. (2008)

Bottom Line: No evidence was found for isolation by distance, and gene flow was bidirectional and of similar magnitude among adjacent populations.In both lineages, the optimum temperature for larval development was at about 23 degrees C, but a clear difference was found at lower temperatures.While larvae of the temperate lineage could complete development at temperatures as low as 12 degrees C, those of the subtropical lineage did not complete development below 17 degrees C.

View Article: PubMed Central - HTML - PubMed

Affiliation: Molecular Ecology and Systematics Group, Botany Department, Rhodes University, 6140 Grahamstown, South Africa. Peter.Teske@bio.mq.edu.au

ABSTRACT

Background: Genetic breaks separating regional lineages of marine organisms with potentially high broadcasting abilities are generally attributed either to dispersal barriers such as currents or upwelling, or to behavioural strategies promoting self-recruitment. We investigated whether such patterns could potentially also be explained by adaptations to different environmental conditions by studying two morphologically distinguishable genetic lineages of the estuarine mudprawn Upogebia africana across a biogeographic disjunction in south-eastern Africa. The study area encompasses a transition between temperate and subtropical biotas, where the warm, southward-flowing Agulhas Current is deflected away from the coast, and its inshore edge is characterised by intermittent upwelling. To determine how this phylogeographic break is maintained, we estimated gene flow among populations in the region, tested for isolation by distance as an indication of larval retention, and reared larvae of the temperate and subtropical lineages at a range of different temperatures.

Results: Of four populations sampled, the two northernmost exclusively included the subtropical lineage, a central population had a mixture of both lineages, and the southernmost estuary had only haplotypes of the temperate lineage. No evidence was found for isolation by distance, and gene flow was bidirectional and of similar magnitude among adjacent populations. In both lineages, the optimum temperature for larval development was at about 23 degrees C, but a clear difference was found at lower temperatures. While larvae of the temperate lineage could complete development at temperatures as low as 12 degrees C, those of the subtropical lineage did not complete development below 17 degrees C.

Conclusion: The results indicate that both southward dispersal of the subtropical lineage inshore of the Agulhas Current, and its establishment in the temperate province, may be limited primarily by low water temperatures. There is no evidence that the larvae of the temperate lineage would survive less well in the subtropical province than in their native habitat, and their exclusion from this region may be due to a combination of upwelling, short larval duration with limited dispersal potential near the coast, plus transport away from the coast of larvae that become entrained in the Agulhas Current. This study shows how methods from different fields of research (genetics, physiology, oceanography and morphology) can be combined to study phylogeographic patterns.

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Map of the sampling area. Samples of the mudprawn Upogebia africana used for genetic analyses came from the four sampling sites indicated in boldface, and those for the larval rearing experiments from the northernmost (Mngazana) and southernmost site (Swartkops). The Haga Haga Estuary is the southernmost site at which mudprawns of the subtropical lineage have so far been recorded, and the Mthatha Estuary the northernmost site at which individuals of the warm-temperate lineage have been found. The chequered area gives the approximate position of cooler water inshore of the Agulhas Current [60]. The insert shows the location of the Wild Coast region in South Africa and the distribution range of U. africana.
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Figure 1: Map of the sampling area. Samples of the mudprawn Upogebia africana used for genetic analyses came from the four sampling sites indicated in boldface, and those for the larval rearing experiments from the northernmost (Mngazana) and southernmost site (Swartkops). The Haga Haga Estuary is the southernmost site at which mudprawns of the subtropical lineage have so far been recorded, and the Mthatha Estuary the northernmost site at which individuals of the warm-temperate lineage have been found. The chequered area gives the approximate position of cooler water inshore of the Agulhas Current [60]. The insert shows the location of the Wild Coast region in South Africa and the distribution range of U. africana.

Mentions: The South African coastline provides several examples of phylogeographic breaks associated with discontinuities in water temperature. These include breaks at Cape Agulhas and Cape Point, both of which separate lineages associated with cool-temperate and warm-temperate biogeographic regions [12-14], a break in the Wild Coast region on the southeast coast that is associated with the boundary of the warm-temperate and subtropical provinces [13,15-17], and a break in the northeast of the country near St Lucia that separates subtropical and tropical lineages [18,19]. While phylogeographic breaks associated with these biogeographic discontinuities are mostly subtle and are based on significant genetic structure or monophyletic mtDNA phylogroups, the Wild Coast case includes examples of lineages for which morphological [15,16] and physiological (Zardi & Nicastro, in prep.) differences have been identified. The oceanography of the Wild Coast is strongly influenced by the warm, southward-flowing Agulhas Current, which lies about 10 km offshore along most of South Africa's east and southeast coast as it follows the narrow continental shelf [20]. Inshore of the current, there are frequent reversals of current direction, with surface water flow being driven predominantly by longshore wind [21]. From about Port Alfred southwards (Fig. 1), the shelf starts to widen and the current is deflected away from the coast (a region hereafter referred to as the Agulhas Current Deflection Zone, or ACDZ). This results in a decreasing influence of the current that manifests itself in sea surface temperatures being cooler south of this point [22]. A persistent, localised upwelling cell is located inshore of the current where the shelf widens, although it does not always affect surface water temperature [23]. Many tropical and subtropical species have been reported in temperate waters beyond the ACDZ, especially during the summer months, but they do not establish themselves permanently [24].


Oceanic dispersal barriers, adaptation and larval retention: an interdisciplinary assessment of potential factors maintaining a phylogeographic break between sister lineages of an African prawn.

Teske PR, Papadopoulos I, Newman BK, Dworschak PC, McQuaid CD, Barker NP - BMC Evol. Biol. (2008)

Map of the sampling area. Samples of the mudprawn Upogebia africana used for genetic analyses came from the four sampling sites indicated in boldface, and those for the larval rearing experiments from the northernmost (Mngazana) and southernmost site (Swartkops). The Haga Haga Estuary is the southernmost site at which mudprawns of the subtropical lineage have so far been recorded, and the Mthatha Estuary the northernmost site at which individuals of the warm-temperate lineage have been found. The chequered area gives the approximate position of cooler water inshore of the Agulhas Current [60]. The insert shows the location of the Wild Coast region in South Africa and the distribution range of U. africana.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2628387&req=5

Figure 1: Map of the sampling area. Samples of the mudprawn Upogebia africana used for genetic analyses came from the four sampling sites indicated in boldface, and those for the larval rearing experiments from the northernmost (Mngazana) and southernmost site (Swartkops). The Haga Haga Estuary is the southernmost site at which mudprawns of the subtropical lineage have so far been recorded, and the Mthatha Estuary the northernmost site at which individuals of the warm-temperate lineage have been found. The chequered area gives the approximate position of cooler water inshore of the Agulhas Current [60]. The insert shows the location of the Wild Coast region in South Africa and the distribution range of U. africana.
Mentions: The South African coastline provides several examples of phylogeographic breaks associated with discontinuities in water temperature. These include breaks at Cape Agulhas and Cape Point, both of which separate lineages associated with cool-temperate and warm-temperate biogeographic regions [12-14], a break in the Wild Coast region on the southeast coast that is associated with the boundary of the warm-temperate and subtropical provinces [13,15-17], and a break in the northeast of the country near St Lucia that separates subtropical and tropical lineages [18,19]. While phylogeographic breaks associated with these biogeographic discontinuities are mostly subtle and are based on significant genetic structure or monophyletic mtDNA phylogroups, the Wild Coast case includes examples of lineages for which morphological [15,16] and physiological (Zardi & Nicastro, in prep.) differences have been identified. The oceanography of the Wild Coast is strongly influenced by the warm, southward-flowing Agulhas Current, which lies about 10 km offshore along most of South Africa's east and southeast coast as it follows the narrow continental shelf [20]. Inshore of the current, there are frequent reversals of current direction, with surface water flow being driven predominantly by longshore wind [21]. From about Port Alfred southwards (Fig. 1), the shelf starts to widen and the current is deflected away from the coast (a region hereafter referred to as the Agulhas Current Deflection Zone, or ACDZ). This results in a decreasing influence of the current that manifests itself in sea surface temperatures being cooler south of this point [22]. A persistent, localised upwelling cell is located inshore of the current where the shelf widens, although it does not always affect surface water temperature [23]. Many tropical and subtropical species have been reported in temperate waters beyond the ACDZ, especially during the summer months, but they do not establish themselves permanently [24].

Bottom Line: No evidence was found for isolation by distance, and gene flow was bidirectional and of similar magnitude among adjacent populations.In both lineages, the optimum temperature for larval development was at about 23 degrees C, but a clear difference was found at lower temperatures.While larvae of the temperate lineage could complete development at temperatures as low as 12 degrees C, those of the subtropical lineage did not complete development below 17 degrees C.

View Article: PubMed Central - HTML - PubMed

Affiliation: Molecular Ecology and Systematics Group, Botany Department, Rhodes University, 6140 Grahamstown, South Africa. Peter.Teske@bio.mq.edu.au

ABSTRACT

Background: Genetic breaks separating regional lineages of marine organisms with potentially high broadcasting abilities are generally attributed either to dispersal barriers such as currents or upwelling, or to behavioural strategies promoting self-recruitment. We investigated whether such patterns could potentially also be explained by adaptations to different environmental conditions by studying two morphologically distinguishable genetic lineages of the estuarine mudprawn Upogebia africana across a biogeographic disjunction in south-eastern Africa. The study area encompasses a transition between temperate and subtropical biotas, where the warm, southward-flowing Agulhas Current is deflected away from the coast, and its inshore edge is characterised by intermittent upwelling. To determine how this phylogeographic break is maintained, we estimated gene flow among populations in the region, tested for isolation by distance as an indication of larval retention, and reared larvae of the temperate and subtropical lineages at a range of different temperatures.

Results: Of four populations sampled, the two northernmost exclusively included the subtropical lineage, a central population had a mixture of both lineages, and the southernmost estuary had only haplotypes of the temperate lineage. No evidence was found for isolation by distance, and gene flow was bidirectional and of similar magnitude among adjacent populations. In both lineages, the optimum temperature for larval development was at about 23 degrees C, but a clear difference was found at lower temperatures. While larvae of the temperate lineage could complete development at temperatures as low as 12 degrees C, those of the subtropical lineage did not complete development below 17 degrees C.

Conclusion: The results indicate that both southward dispersal of the subtropical lineage inshore of the Agulhas Current, and its establishment in the temperate province, may be limited primarily by low water temperatures. There is no evidence that the larvae of the temperate lineage would survive less well in the subtropical province than in their native habitat, and their exclusion from this region may be due to a combination of upwelling, short larval duration with limited dispersal potential near the coast, plus transport away from the coast of larvae that become entrained in the Agulhas Current. This study shows how methods from different fields of research (genetics, physiology, oceanography and morphology) can be combined to study phylogeographic patterns.

Show MeSH