Population genetic structure of the perlemoen Haliotis midae in South Africa: evidence of range expansion and founder events
TL;DR: It is concluded that populations of H. midae on either side of Cape Agulhas represent 2 independent reproductive stocks, and the area of transition between the stocks coincides with oceanographic features of the region.
Abstract: Genetic diversity in Haliotis midae, a highly valued and heavily exploited marine gastropod, was assessed using 3 marker types across samples from the species' range in South Africa. Variation was compared at 7 allozyme loci, 2 regions of mitochondrial DNA and 3 microsatellite loci. We conclude that populations of H. midae on either side of Cape Agulhas represent 2 independent reproductive stocks. The area of transition between the stocks coincides with oceanographic features of the region. Evidence from all 3 types of genetic marker indicates an isolated introduction event to the east of Cape Agulhas, and subsequent range expansion in an easterly direction. The disparity between allozyme data and the other 2 forms is seen as further evidence for the presence of balanc- ing selection at allozyme loci.
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TL;DR: A meta-analysis refutes recent reviews and conventional wisdom that pelagic larval duration (PLD) is a good predictor of the magnitude of gene flow and geo- graphic scale of population structure in marine systems.
Abstract: Population connectivity plays significant roles on both evolutionary and ecological time-scales; however, quantifying the magnitude and pattern of ex- change between populations of marine organisms is hindered by the difficulty of tracking the trajectory and fate of propagules. We explored biophysical correlates of population substructure to determine how well pelagic larval duration (PLD) correlates with population genetic estimates of connectivity in a sample of 300 published studies drawn pseudo-randomly from about 1600 hits on electronic searches. In direct contrast to the general expectation of a strong correlation, we find that average PLD is poorly correlated (r 2 < 0.1) with genetic structure (FST). Furthermore, even this weak correlation is anchored by non-pelagic dispersal, because removal of the zero PLD class (direct developers) from the analy- sis resulted in a non-significant relationship between FST and PLD. For species in which minimum, maximum, and mean PLDs were available, it is noteworthy that both minimum and maximum PLDs are better corre- lated with FST than the mean larval duration, which has been used in all such previous studies. A 3-way AN- COVA reveals that genetic marker class (allozymes, microsatellites, and mitochondrial DNA sequences), as opposed to habitat or swimming ability, explain most of the variation in FST (F = 7.113, df = 2, p = 0.001), with higher values of FST obtained from mtDNA than with either microsatellites or allozymes (which were not sig- nificantly different). Our meta-analysis refutes recent reviews and conventional wisdom that PLD is a good predictor of the magnitude of gene flow and geo- graphic scale of population structure in marine systems.
512 citations
TL;DR: This review describes the state of marine phylogeography in southern Africa, that is, the study of evolutionary relationships at the species level, or amongst closely related species, in relation to the region’s marine environment, and focuses particularly on coastal phylegeography.
Abstract: The southern African marine realm is located at the transition zone between the Atlantic and Indo-Pacific biomes. Its biodiversity is particularly rich and comprises faunal and floral elements from the two major oceanic regions, as well as a large number of endemics. Within this realm, strikingly different biota occur in close geographic proximity to each other, and many of the species with distributions spanning two or more of the region’s marine biogeographic provinces are divided into evolutionary units that can often only be distinguished on the basis of genetic data. In this review, we describe the state of marine phylogeography in southern Africa, that is, the study of evolutionary relationships at the species level, or amongst closely related species, in relation to the region’s marine environment. We focus particularly on coastal phylogeography, where much progress has recently been made in identifying phylogeographic breaks and explaining how they originated and are maintained. We also highlight numerous shortcomings that should be addressed in the near future. These include: the limited data available for commercially important organisms, particularly offshore species; the paucity of oceanographic data for nearshore areas; a dearth of studies based on multilocus data; and the fact that studying the role of diversifying selection in speciation has been limited to physiological approaches to the exclusion of genetics. It is becoming apparent that the southern African marine realm is one of the world’s most interesting environments in which to study the evolutionary processes that shape not only regional, but also global patterns of marine biodiversity.
186 citations
TL;DR: A landscape genetic approach was used to detect areas of low gene flow using a joint analysis of spatial and genetic information, and a novel approach of using particle tracking software to mimic scallop larval dispersal was employed to interpret within‐region genetic patterns.
Abstract: Marine bivalves are sessile or sedentary as adults but have planktonic larvae which can potentially disperse over large distances. Consequently larval transport is expected to play a prominent role in facilitating gene flow and determining population structure. The sea scallop (Placopecten magellanicus) is a dioecious species with high fecundity, broadcast spawning and a c. 30-day planktonic larval stage, yet it forms discrete populations or 'beds' which have significantly different dynamics and characteristics. We analysed variation at six microsatellite loci in 12 locations throughout the geographic range of the species from Newfoundland, Canada, to New Jersey, USA. Significant differentiation was present and the maximum pairwise theta value, between one of the Newfoundland samples in the north and a sample from the southern portion of the range, was high at 0.061. Other proximate pairs of samples had no detectable genetic differentiation. Mantel tests indicated a significant isolation by distance, but only when one of the populations was excluded. A landscape genetic approach was used to detect areas of low gene flow using a joint analysis of spatial and genetic information. The two major putative barriers inferred by Monmonier's algorithm were then used to define regions for an analysis of molecular variance (amova). That analysis showed a significant but low percentage (1.2%) of the variation to be partitioned among regions, negligible variation among populations within regions, and the majority of the variance distributed between individuals within populations. Prominent currents were concordant with the demarcation of the regions, while a novel approach of using particle tracking software to mimic scallop larval dispersal was employed to interpret within-region genetic patterns.
129 citations
Cites background or result from "Population genetic structure of the..."
...…strategy to the sea scallop, also exhibit an excess of homozygosity which has been generally explained by inbreeding (Brown 1991; Hara & Kikuchi 1992; Huang et al. 2000; Withler et al. 2003), although null alleles have been inferred from some species (e.g. Haliotis midae: Evans et al. 2004)....
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...This level of differentiation is consistent with the mean FST for marine fish (0.062; Ward et al. 1994; Waples 1998) and comparable to that found over similar geographic scales in the abalone Haliotis midae (FST = 0.067; Evans et al. 2004)....
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TL;DR: The amount of genetic structure within marine biogeographic regions strongly depends on the presence or absence of free-swimming larvae, and whether or not they are capable of active dispersal seems to have little effect on connectivity among populations.
Abstract: The amount of genetic structure in marine invertebrates is often thought to be negatively correlated with larval duration. However, larval retention may increase genetic structure in species with long-lived planktonic larvae, and rafting provides a means of dispersal for species that lack a larval dispersal phase. We compared genetic structure, demographic histories and levels of gene flow of regional lineages (in most cases defined by biogeographic region) of five southern African coastal invertebrates with three main types of larval development: (1) dispersal by long-lived planktonic larvae (mudprawn Upogebia africana and brown mussel Perna perna), (2) abbreviated larval development (crown crab Hymenosoma orbiculare) and (3) direct development (estuarine isopod Exosphaeroma hylecoetes and estuarine cumacean Iphinoe truncata). We hypothesized that H. orbiculare, having abbreviated larval development, would employ a strategy of larval retention, resulting in genetic structure comparable to that of the direct developers rather than the planktonic dispersers. However, regional population structure was significantly lower in all species with planktonic larvae, including H. orbiculare, than in the direct developers. Moreover, nested clade analysis identified demographic histories resulting from low levels of gene flow (isolation by distance and allopatric fragmentation) in the direct developers only, and migration rates were significantly higher in all three species having planktonic larvae than in the direct developers. We conclude that the amount of genetic structure within marine biogeographic regions strongly depends on the presence or absence of free-swimming larvae. Whether such larvae are primarily exported or retained, whether they have long or short larval duration, and whether or not they are capable of active dispersal seems to have little effect on connectivity among populations.
110 citations
Cites background from "Population genetic structure of the..."
...…patterns along the southern African coastline revealed that coastal invertebrate species may be divided into two to three major lineages that in most species are associated with marine biogeographic provinces (e.g. Ridgway et al. 1999; Evans et al. 2004; Teske et al. 2006; Zardi et al. 2007)....
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TL;DR: Ecological factors and modes of dispersal are likely to have played a role in both cladogenesis of the different lineages and in the establishment of their present-day distribution patterns.
Abstract: The South African coastline comprises 3 main biogeographic provinces: (1) the cool- temperate west coast, (2) the warm-temperate south coast, and (3) the subtropical east coast. The boundaries between these regions are defined by changes in species compositions and hydrological conditions. It is possible that these affect phylogeographic patterns of coastal organisms differently, depending on the species' ecologies and modes of dispersal. In the present study, genealogies of 3 estuarine crustaceans, each characterized by a different mode of passive dispersal and present in more than one biogeographic province, were reconstructed using mtDNA COI sequences, and the impacts of biogeographic boundaries on their phylogeographic patterns were compared. The species were (mode of dispersal in brackets): (1) the mudprawn Upogebia africana (planktonic larvae), (2) the isopod Exosphaeroma hylecoetes (adult rafting), and (3) the cumacean Iphinoe truncata (adult drift- ing). Two major mtDNA lineages with slightly overlapping distributions were identified in U. africana (the species with the highest dispersal potential). The other 2 species had 3 mtDNA lineages each, which were characterized by strict geographic segregation. Phylogeographic breaks in U. africana and E. hylecoetes coincided with biogeographic boundaries, whereas the phylogeographic patterns identified in I. truncata may reflect persistent palaeogeographic patterns. Ecological factors and modes of dispersal are likely to have played a role in both cladogenesis of the different lineages and in the establishment of their present-day distribution patterns.
97 citations
Cites background from "Population genetic structure of the..."
...This is supported by the fact that the South African abalone Haliotis midae (also a planktonic disperser) comprises 2 reproductive stocks, which are separated by Cape Agulhas and share some haplotypes (Evans et al. 2004)....
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...Evans et al. (2004) showed that mtDNA or microsatellites have greater potential to detect genetic structure, but little phylogeographic work using these markers has been done to date (e.g. Teske et al. 2003, Evans et al. 2004, Tolley et al. 2005)....
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References
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TL;DR: It is argued that many species, which were formerly thought to be unstructured, are in fact subdivided into genetically discrete groups and that the combination of molecular assays of both nuclear and mitochondrial DNA and allozyme loci provides the best approach to understanding the evolutionary dynamics of these interacting populations.
114 citations
01 Jan 1999
TL;DR: The area cladogram, which treats the distribution of the individual species as characters and the areas as taxa, is in general agreement with an unrooted phylogenetic tree of the taxa for which the geographic occurrence is superimposed.
Abstract: The distribution of all 56 abalone species is documented based on specimen records. The three models for the origin of the family (Pacific Rim, Indo-Pacific, Tethys) are evaluated. The area cladogram, which treats the distribution of the individual species as characters and the areas as taxa, is in general agreement with an unrooted phylogenetic tree of the taxa for which the geographic occurrence is superimposed. The basal node of the area cladogram is a fairly large polytomy uniting rather distant provinces such as the north Pacific, Australia, and Africa. A similar pattern emerges from the taxon cladogram. Accordingly, a very general Indo-Pacific origin emerges, best in agreement with the Indo-Pacific model for the origin of the family. The apparent discrepancy with the fossil record is discussed. Although the earliest fossils from the Upper Creatceous have been found in the Caribbean and in California, a major hiatus of on the order of 200 million years can easily account for the discrepancy between the earliest fosssils and the biogeographical reconstruction, as well as for the large basal polytomy in the biogeographical analysis. All species are illustrated, including some distinct juvenile forms, and 30 photographs of live animals. riassunto: Distribuzione e Biogeografìa delle Haliotidae (Gastropoda: Vetigastropoda) recenti. Le Haliotidae comprendono 56 specie recenti descritte, distribuite su scala mondiale, nelle aree temperate e tropicali di entrambi gli emisferi. La distribuzione di tutte le 56 specie è qui illustrata da mappe digitalizzate, sulla base dell'esame oggettivo di esemplari e dell'analisi critica dei dati di letteratura. Sono quindi esaminati i tre modelli proposti per l'origine della famiglia: "Pacific Rim", Indo-Pacifico e Tetisiano. Il cladogramma di area, che tratta le distribuzioni delle singole specie come caratteri e le aree come OTUs, è in accordo generale con un albero filogenetico delle specie (derivato dall'analisi cladistica di dati molecolari ed allozimici) su cui vengano sovrimposte le distribuzioni geografiche. Il nodo basale del cladogramma di area è una politomia piuttosto ampia che riunisce provincie relativamente distanti come il Nord-Pacifico, l'Australia e l'Africa. Un quadro simile emerge dal cladogramma dei taxa. Sulla base dell'analisi di tali cladogrammi emerge un'origine generale Indo-Pacifica del gruppo, che sembrerebbe supportare il modello Indo-Pacifico di origine delle Haliotidae. Vi è un'apparente discrepanza tra questi dati e la loro susseguente interpretazione da una parte, e il record fossile dall'altra. I fossili più antichi noti provengono infatti dal Cretaceo Superiore dei Caraibi e della California. Ciononostante viene discusso come uno iato dell'ordine di 200 milioni di anni possa facilmente spiegare la discrepanza tra i fossili più antichi e la ricostruzione biogeografica più plausibile; si darebbe così anche ragione dell'ampia politomia basale nelle analisi cladistiche. Tutte le specie sono illustrate, con alcune distinte forme giovanili caratterizzate e 30 fotografie di animali viventi. Daniel L. Geiger, Molecular Systematic! Lab, Naturai History Museum of Los Angeles University, Los Angeles, CA 90007, USA; e-mail dgeiger@nmh.org INTRODUCTION Abalone are a family of marine gastropods consisting of 56 currently described species of world-wide distribution in tropical and temperate waters of both hemispheres. During revision work on this family I have recently evaluated all Recent taxa, 200 at the species level and 17 at the genus level (Geiger, 1998a). Some other taxonomic matters have been dealt with elsewhere (Geiger 1998b, 1999; Geiger & Stewart, 1998, Stewart & Geiger, 1999). Knowledge of the distribution of most species is sketchy, particularly due to the absence of specimen based accounts. Most indications in the literature may be termed intuitive (e.g., Ubaldi, 1993, 1995) with limited exceptions (Geiger, 1996, 1999; Simone, 1998; Stewart & Geiger, 1999). In this second, larger treatment of the family Haliotidae, I concentrate on the distributional pattern of all Recent species, including a biogeographical analysis. To date, studies on the biogeography ol the family are marked by their anecdotal nature. Three hypotheses (Fig. 1) for the origin have been proposed and have been discussed by Geiger & Groves (1999) in a review of fossil abalone. Model 1 (Fig. 1A): Pacific Rim. An arc spanning from Japan to northeastern Australia has been identified by Talmadge (1963) as a likely cradle of the family. From this nuclear distribution abalone then dispersed in a star shaped pattern to the northwestern and then northeastern Pacific, to Australia and the Indian Ocean. The basis of this model was never made explicit. Model 2 (Fig. IB): Indo-Pacific. The highest present day diversity of the family is found in the Indo-Malayan area. Although it is well appreciated that the correlation of high present day diversity with origin of the group in question is highly problematic, it provides one possible center of radiation for the family, and was discussed by LlNDBERG (1992) and BRIGGS
107 citations
TL;DR: Based on these results, rates of recolonization and recovery of locally depressed or extirpated black abalone populations are likely to be slow despite harvest restrictions.
91 citations
Additional excerpts
...Hamm & Burton (2000) reported a similar value at allozyme loci in Haliotis cracherodii (FST = 0.039), but that differentiation was, however, not supported by mtDNA data collected from the same samples....
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TL;DR: It is concluded that zones of about 500 km of coastline, corresponding to 'neighbourhood size', could be recognized for the conservation of regional gene pools, but that stock-recruitment relationships need to be established on a localized basis.
Abstract: Populations of blacklip abalone (Haliotis rubra) from southern Australia have been investigated genetically using protein gel electrophoresis. Allele frequency and genotype distributions were analysed to provide information on population structure, gene flow patterns and genetic differentiation among local populations. Breeding populations appear to be large. Measures of genetic distance reveal an 'isolation by distance' broad-scale population structure, although significant genetic heterogeneity can occur between sites < 3 km apart. Reasons for this apparent contradiction are discussed. It is concluded that zones of about 500 km of coastline, corresponding to 'neighbourhood size', could be recognized for the conservation of regional gene pools, but that stock-recruitment relationships need to be established on a localized basis.
78 citations
TL;DR: It is inferred that the lake populations of G. truttaceus have probably experienced at least one, severe, but transitory bottleneck possibly induced by natural selection for life-history characters essential for survival in the lacustrine habitat.
Abstract: Galaxias truttaceus is found in coastal rivers and streams in south-eastern Australia. It spawns at the head of estuaries in autumn and the larvae spend 3 months of winter at sea before returning to fresh water. In Tasmania there are landlocked populations of G. truttaceus in a cluster of geologically young lakes on the recently glaciated Central Plateau. These populations have no marine larval stage and spawn in the lakes in spring. Speciation due to land locking is thought to be a frequent occurrence within Galaxias. To investigate the nature of the speciation event which may be occurring within lake populations of G. truttaceus we studied the mitochondrial DNA (mtDNA) and allozyme diversity of both lake and stream populations. Using the presence or absence of restriction sites recognized by 13 six-base restriction endonucleases, we found 58 mtDNA haplotypes among 150 fish collected from 13 Tasmanian and one south-east Australian mainland stream populations. The most parsimonious network relating the haplotypes by site loss or gain was starlike in shape. We argue that this arrangement is best explained by selection upon slightly beneficial mutations within the mitochondrial genome. Gene diversity analysis under Wright's island model showed that the populations in each drainage were not genetically subdivided. Only two of these stream haplotypes were found among the 66 fish analyzed from four lake populations. Despite the extreme lack of mtDNA diversity in lake populations, the observed nuclear DNA heterozygosity of 40 lake fish (0.10355) was only slightly less than that of 82 stream fish (0.11635). In the short time (3000-7000 years) that the lake fish have been landlocked, random genetic drift in a finite, stable-sized population was probably not responsible for the lack of mtDNA diversity in the lake populations. We infer the lake populations have probably experienced at least one, severe, but transitory bottleneck possibly induced by natural selection for life-history characters essential for survival in the lacustrine habitat. If speciation is occurring in the landlocked populations of G. truttaceus, then it may be driven by genetic transilience.
78 citations