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: The results seem, overall, to agree well with neutralist expectations for species with large, stable population sizes and the mean heterozygosities, their variances and the observed and expected proportions of polymorphic loci seem to fit well with predictions based on the neutralist hypothesis.
Abstract: The predictions of neutralist and selectionist hypotheses have been tested many times in the past, but mostly using data only from organisms such as vertebrates, with generally low to average heterozygosities. The more recent discovery of particularly high levels of genetic variation in marine sponges and coelenterates provides an opportunity to use data from such species to contribute further to the understanding of the determinants of heterozygosity in natural populations. Therefore, 23 species of sponges and coelenterates from temperate, tropical and boreal waters were analysed by gel electrophoresis for an average of 14.3 enzyme loci per species.
Mean heterozygosity values for each species were unusually high, ranging between 0.106 and 0.401. The means and variances of the heterozygosity estimates showed reasonable correlation with neutralist predictions (with both the stepwise mutation and the infinite alleles models). Population sizes were generally difficult to estimate with any confidence, but, for one sponge species for which this was possible, levels of heterozygosity again were similar to neutralist predictions, although the same was not apparently true for three species of sea anemone. No differences were found between heterozygosity levels of tropical and temperate species of sponges and coelenterates, thus apparently contradicting the selectionist ‘trophic resource stability’ and ‘temporal environmental variation’ hypotheses. Conversely, however, the consistently high levels of genetic variation found in coelenterates and sponges may be argued to be related to common biological characteristics, such as sessile life, great evolutionary ‘age’, limited ability to disperse and probable low homoeostatic capability.
Our results seem, overall, to agree well with neutralist expectations for species with large, stable population sizes. Also, the mean heterozygosities, their variances and the observed and expected proportions of polymorphic loci seem to fit well with predictions based on the neutralist hypothesis. However, the selectionist ‘environmental grain’ and the ‘shifting balance’ hypotheses fit the data equally well. As with much earlier work, the problems in distinguishing between the various predictions of selectionist or neutralist ideas make it both difficult and unwise to draw definite conclusions.
65 citations
TL;DR: Genetic variation within species assayed by molecular tools has been useful in examining the stability of populations through time and in assessing patterns of recruitment to geographically separated populations, and enhanced understanding of these ecological problems will also require intensive spatial and temporal monitoring of both larval and adult populations.
54 citations
TL;DR: The results from both techniques suggest restricted gene flow between blacklip abalone separated by Bass Strait, and homogeneity among geographically isolated samples from around the island of Tasmania.
Abstract: Genetic variation in five geographically isolated samples of the blacklip abalone, Haliotis rubra, from south-eastern Australia was examined using two molecular techniques. A restriction fragment length polymorphism (RFLP) analysis using six restriction enzymes on the ND3/COIII region of mitochondrial DNA was compared with five independent nuclear DNA microsatellite loci. The results from both techniques suggest restricted gene flow between blacklip abalone separated by Bass Strait, and homogeneity among geographically isolated samples from around the island of Tasmania. Although both techniques showed similar resolving power, microsatellite DNA analysis is the preferred molecular technique for the fine scale investigation of blacklip abalone population structure because it makes possible the examination of numerous independent loci with potentially high levels of polymorphism. Both sample and locus specific homozygote excesses were recorded for the microsatellite loci. The most likely explanation for the locus specific deviations from Hardy-Weinberg expectations is the presence of null alleles.
35 citations
TL;DR: In this article, the mtDNA sequences yielded highly variable levels of divergence, ranging from 0.0 to 8.8% within populations, and 0.5 to 9.8 % among populations.
Abstract: Research over the past 20 years has shown, with the help of molecular markers, that the population genetics and distribution patterns of freshwater invertebrates in North America are often more complex than was previously believed. Here we extend this research to an, as yet, unstudied but widespread and common group, the freshwater bryozoans. Colonies of the bryozoan Cristatella mucedo were collected from a number of lakes across central North America, and were characterized genetically by analysis of microsatellite loci and mitochondrial DNA (mtDNA) cytochrome b sequences. The microsatellites illustrate a pattern of generally diverse and highly differentiated populations that contain little evidence of recent gene flow. The mtDNA sequences yielded highly variable levels of divergence, ranging from 0.0 to 8.8% within populations, and 0.0 to 9.8% among populations. The multiple divergent mtDNA lineages within populations provide evidence for repeated colonization events. The lack of clustering of haplotypes by site suggests that there has been widespread dispersal of multiple genetic lineages since the last ice age. While some of the haplotype lineages may have evolved in disjunct glacial refugia, the maximum levels of divergence predate the time since the last glacial-interglacial cycles. It is likely that multiple factors including vicariance events, patterns of dispersal, localized extinction, and an unusual life history, explain the unique phylogeographic patterns evident today in populations of C. mucedo.
30 citations
"Population genetic structure of the..." refers background in this paper
...There are 5 recognised species of abalone on the South African coast (Geiger 2000)....
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