Sophie von der Heyden

Significant population structure and asymmetric gene flow patterns amidst expanding populations of Clinus cottoides (Perciformes, Clinidae): application of molecular data to marine conservation planning in South Africa

Clinus cottoides is a fish endemic to the coast of South Africa, predominantly inhabiting rock pools. All South African clinids are viviparous, but probably breed throughout the year; as such, their dispersal may be limited, unlike species with pelagic larval stages. We analysed 343 fish from 14 localities on the west, south and east coasts using two mitochondrial genes and the second intron of the S7 ribosomal gene. Mitochondrial DNA analyses recovered significant genetic differentiation between fish populations from the east coast and other sampling locations, with a second break found between Gansbaai and Cape Agulhas on the south coast. Nuclear DNA recovered shallower, but significant, levels of population structure. Coalescent analyses suggested remarkably asymmetrical gene flow between sampling locations, suggesting that the cold Atlantic Benguela Current and Indian Ocean Agulhas counter‐current play important roles in facilitating dispersal. There was no gene flow between the east coast and the other sites, suggesting that these populations are effectively isolated. Divergence times between them were estimated to at least 68 000 years. Neutrality tests and mismatch distributions suggest recent population expansions, with the exception of peripheral western and eastern populations (possibly a consequence of environmental extremes at the edge of the species distribution). Analyses of the current South African marine protected areas network show that it is not connected and that De Hoop, one of South Africas largest marine reserves, appears to be an important source population of recruits to both the south and southwest coasts.

A synthesis of genetic connectivity in deep‐sea fauna and implications for marine reserve design

With anthropogenic impacts rapidly advancing into deeper waters, there is growing interest in establishing deep‐sea marine protected areas (MPAs) or reserves. Reserve design depends on estimates of connectivity and scales of dispersal for the taxa of interest. Deep‐sea taxa are hypothesized to disperse greater distances than shallow‐water taxa, which implies that reserves would need to be larger in size and networks could be more widely spaced; however, this paradigm has not been tested. We compiled population genetic studies of deep‐sea fauna and estimated dispersal distances for 51 studies using a method based on isolation‐by‐distance slopes. Estimates of dispersal distance ranged from 0.24 km to 2028 km with a geometric mean of 33.2 km and differed in relation to taxonomic and life‐history factors as well as several study parameters. Dispersal distances were generally greater for fishes than invertebrates with the Mollusca being the least dispersive sampled phylum. Species that are pelagic as adults were more dispersive than those with sessile or sedentary lifestyles. Benthic species from soft‐substrate habitats were generally less dispersive than species from hard substrate, demersal or pelagic habitats. As expected, species with pelagic and/or feeding (planktotrophic) larvae were more dispersive than other larval types. Many of these comparisons were confounded by taxonomic or other life‐history differences (e.g. fishes being more dispersive than invertebrates) making any simple interpretation difficult. Our results provide the first rough estimate of the range of dispersal distances in the deep sea and allow comparisons to shallow‐water assemblages. Overall, dispersal distances were greater for deeper taxa, although the differences were not large (0.3–0.6 orders of magnitude between means), and imbalanced sampling of shallow and deep taxa complicates any simple interpretation. Our analyses suggest the scales of dispersal and connectivity for reserve design in the deep sea might be comparable to or slightly larger than those in shallow water. Deep‐sea reserve design will need to consider the enormous variety of taxa, life histories, hydrodynamics, spatial configuration of habitats and patterns of species distributions. The many caveats of our analyses provide a strong impetus for substantial future efforts to assess connectivity of deep‐sea species from a variety of habitats, taxonomic groups and depth zones.

Mitochondrial DNA variation of the west-coast rock lobster, Jasus lalandii: marked genetic diversity differences among sampling sites

Jasus lalandii (Milne-Edwards 1837), the west-coast rock lobster, occurs in the shallow, cool–temperate waters along the south and west coasts of southern Africa. This species has a long history of intensive exploitation, which has had a significant impact on population numbers in the past. To enhance our current understanding of lobster population structuring, genetic data from the mitochondrial (mt) DNA 16S rRNA gene was generated for 235 adult individuals collected at eight sampling sites. Most individuals (59.6%) share a common haplotype and 35 unique haplotypes were dispersed throughout the range. In total, 97.2% of the variation was found among individuals within sampling sites and 2.8% was among sites. Pairwise ΦST analyses revealed shallow, yet significant structure between Hout Bay individuals and some other sampling sites. The J. lalandii haplotype network indicates a starlike structure with no geographic signal; however, genetic diversity sharply decreases towards the edges of the species distribution. The general lack of phylogeographic structure among J. lalandii populations probably results from the absence of strong barriers to larval dispersal. Based on our mtDNA data there is no justification for the recognition of separate fishing stocks, but the high genetic diversities of populations at Hout Bay and Cape Hangklip, the latter currently outside of marine protected areas, makes these populations critical to conservation efforts.

Variation in palaeo-shorelines explains contemporary population genetic patterns of rocky shore species

Processes driving and maintaining disjunct genetic populations in marine systems are poorly understood, owing to a lack of evidence of hard barriers that could have shaped patterns of extant population structure. Here, we map two genetically divergent lineages of an obligate rocky shore fish, Clinus cottoides, and model sea-level change during the last 110 000 years to provide the first evidence of a vicariant event along the southern coastline of Africa. Results reveal that lowered sea levels during glacial periods drastically reduced rocky intertidal habitat, which may have isolated populations in two refugia for at least 40 000 years. Contemporary coastal dynamics and oceanography explain secondary contact between lineages. This scenario provides an explanation for the origin of population genetic breaks despite a lack of obvious present-day geographical barriers and highlights the need for including palaeo-oceanography in unravelling extant population patterns.

The influence of pleistocene climatic changes and ocean currents on the phylogeography of the Southern African Barnacle, Tetraclita serrata (Thoracica; Cirripedia)

The evolutionary effects of glacial periods are poorly understood for Southern Hemisphere marine intertidal species, particularly obligatory sessile organisms. We examined this by assessing the phylogeographic patterns of the southern African volcano barnacle, Tetraclita serrata, a dominant species on rocky intertidal shores. Restricted gene flow in some geographical areas was hypothesized based on oceanic circulation patterns and known biogeographic regions. Barnacle population genetic structure was investigated using the mitochondrial cytochrome oxidase subunit 1 (COI) region for 410 individuals sampled from 20 localities spanning the South African coast. The mtDNA data were augmented by generating nuclear internal transcribed spacer 1 (ITS1) sequences from a subset of samples. Phylogenetic and population genetic analyses of mitochondrial DNA data reveal two distinct clades with mostly sympatric distributions, whereas nuclear analyses reveal only a single lineage. Shallow, but significant structure (0.0041–0.0065, P<0.01) was detected for the mtDNA data set, with the south-west African region identified as harbouring the highest levels of genetic diversity. Gene flow analyses on the mtDNA data show that individuals sampled in south-western localities experience gene flow primarily in the direction of the Benguela Current, while south and eastern localities experience bi-directional gene flow, suggesting an influence of both the inshore currents and the offshore Agulhas Current in the larval distribution of T. serrata. The mtDNA haplotype network, Bayesian Skyline Plots, mismatch distributions and time since expansion indicate that T. serrata population numbers were not severely affected by the Last Glacial Maximum (LGM), unlike other southern African marine species. The processes resulting in the two morphologically cryptic mtDNA lineages may be the result of a recent historical allopatric event followed by secondary contact or could reflect selective pressures due to differing environmental conditions.

High connectivity and lack of mtDNA differentiation among two previously recognized spiny lobster species in the southern Atlantic and Indian Oceans

Abstract Adult spiny lobsters Jasus paulensis and J. tristani inhabit non-emergent seamounts and remote islands in the southern mid-latitude (30–45°S) Indian and Atlantic Oceans. Populations are often thousands of kilometres apart, and metapopulation genetic structure relies on successful exchange of long-lived drifting larvae. Genetic population structure and connectivity were investigated by sequencing the mitochondrial cytochrome oxidase I gene from lobsters collected at two Indian Ocean sites (Seamount 150 and St Paul/Amsterdam Islands) and two Atlantic sites (Vema Seamount and Gough/Inaccessible Islands) between 2006 and 2011. Jasus paulensis and J. tristani individuals share identical haplotypes across the distribution range and Bayesian phylogenetic analyses strongly support the monophyly of all individuals sampled, to the exclusion of all other recognized Jasus species. Analyses of molecular variance revealed no significant population genetic differentiation between sites, and Fus F s and a mismatch distribution suggested demographic expansion, which was estimated to have occurred between 14,000 and 118,000 years ago. The results show an apparent lack of barriers to dispersal and gene flow over thousands of kilometres of the southern Indian and Atlantic Oceans, and suggest that J. paulensis and J. tristani should be synonymized as J. paulensis (Heller, 1862).

Spatio‐temporal genetic structure and the effects of long‐term fishing in two partially sympatric offshore demersal fishes

Environmental gradients have been shown to disrupt gene flow in marine species, yet their influence in structuring populations at depth remains poorly understood. The Cape hakes (Merluccius paradoxus and M. capensis) are demersal species co‐occurring in the Benguela Current system, where decades of intense fishing resulted in severely depleted stocks in the past. Previous studies identified conflicting mtDNA genetic substructuring patterns and thus contrasting evolutionary trajectories for both species. Using 10 microsatellite loci, the control region of mtDNA and employing a seascape genetics approach, we investigated genetic connectivity and the impact of prolonged exploitation in the two species, which are characterized by different patterns of fishing pressure. Three consecutive years were sampled covering the entire distribution (N = 2100 fishes). Despite large estimated population sizes, both species exhibited low levels of contemporary genetic diversity (0.581 < HE < 0.692), implying that fishing has had a significant impact on their genetic composition and evolutionary trajectories. Further, for M. paradoxus, significant temporal, but not spatial, divergence points to the presence of genetic chaotic patchiness. In contrast, M. capensis exhibited a clear latitudinal cline in genetic differentiation between Namibia and South Africa (FST = 0.063, P < 0.05), with low (0.2% per generation) estimates of contemporary gene flow. Seascape analyses reveal an association with bathymetry and upwelling events, suggesting that adaptation to local environmental conditions may drive genetic differentiation in M. capensis. Importantly, our results highlight the need for temporal sampling in disentangling the complex factors that impact population divergence in marine fishes.

A Review of Molecular Approaches for Investigating Patterns of Coevolution in Marine Host–Parasite Relationships

Parasites and their relationships with hosts play a crucial role in the evolutionary pathways of every living organism. One method of investigating host-parasite systems is using a molecular approach. This is particularly important as analyses based solely on morphology or laboratory studies of parasites and their hosts do not take into account historical evolutionary interactions that can shape the distribution, abundance and population structure of parasites and their hosts. However, the predominant host-parasite coevolution literature has focused on terrestrial hosts and their parasites, and there still is a lack of studies in marine environments. Given that marine systems are generally more open than terrestrial ones, they provide fascinating opportunities for large-scale (as well as small-scale) geographic studies. Further, patterns and processes of genetic structuring and systematics are becoming more available across many different taxa (but especially fishes) in many marine systems, providing an excellent basis for examining whether parasites follow host population/species structure. In this chapter, we first highlight the factors and processes that challenge our ability to interpret evolutionary patterns of coevolution of hosts and their parasites in marine systems at different spatial, temporal and taxonomic scales. We then review the use of the most commonly utilized genetic markers in studying marine host-parasite systems. We give an overview and discuss which molecular methodologies resolve evolutionary relationships best and also discuss the applicability of new approaches, such as next-generation sequencing and studies utilizing functional markers to gain insights into more contemporary processes shaping host-parasite relationships.

Multispecies genetic objectives in spatial conservation planning.

Growing threats to biodiversity and global alteration of habitats and species distributions make it increasingly necessary to consider evolutionary patterns in conservation decision making. Yet, there is no clear-cut guidance on how genetic features can be incorporated into conservation-planning processes, despite multiple molecular markers and several genetic metrics for each marker type to choose from. Genetic patterns differ between species, but the potential tradeoffs among genetic objectives for multiple species in conservation planning are currently understudied. We compared spatial conservation prioritizations derived from 2 metrics of genetic diversity (nucleotide and haplotype diversity) and 2 metrics of genetic isolation (private haplotypes and local genetic differentiation) in mitochondrial DNA of 5 marine species. We compared outcomes of conservation plans based only on habitat representation with plans based on genetic data and habitat representation. Fewer priority areas were selected for conservation plans based solely on habitat representation than on plans that included habitat and genetic data. All 4 genetic metrics selected approximately similar conservation-priority areas, which is likely a result of prioritizing genetic patterns across a genetically diverse array of species. Largely, our results suggest that multispecies genetic conservation objectives are vital to creating protected-area networks that appropriately preserve community-level evolutionary patterns.

When homoplasy mimics hybridization : a case study of Cape hakes (Merluccius capensis and M. paradoxus)

In the marine environment, an increasing number of studies have documented introgression and hybridization using genetic markers. Hybridization appears to occur preferentially between sister-species, with the probability of introgression decreasing with an increase in evolutionary divergence. Exceptions to this pattern were reported for the Cape hakes (Merluccius capensis and M. paradoxus), two distantly related Merluciidae species that diverged 3–4.2 million years ago. Yet, it is expected that contemporary hybridization between such divergent species would result in reduced hybrid fitness. We analysed 1,137 hake individuals using nine microsatellite markers and control region mtDNA data to assess the validity of the described hybridization event. To distinguish between interbreeding, ancestral polymorphism and homplasy we sequenced the flanking region of the most divergent microsatellite marker. Simulation and empirical analyses showed that hybrid identification significantly varied with the number of markers, model and approach used. Phylogenetic analyses based on the sequences of the flanking region of Mmerhk-3b, combined with the absence of mito-nuclear discordance, suggest that previously reported hybridization between M. paradoxus and M. capensis cannot be substantiated. Our findings highlight the need to conduct a priori simulation studies to establish the suitability of a particular set of microsatellite loci for detecting multiple hybridization events. In our example, the identification of hybrids was severely influenced by the number of loci and their variability, as well as the different models employed. More importantly, we provide quantifiable evidence showing that homoplasy mimics the effects of heterospecific crossings which can lead to the incorrect identification of hybridization.