Peter R. Teske

Phylogeographic structure of the caridean shrimp Palaemon peringueyi in South Africa: further evidence for intraspecific genetic units associated with marine biogeographic provinces

Recent genetic studies have shown that most widely distributed, passively dispersing invertebrates in southern Africa have regional intraspecific units that are associated with the three main marine biogeographic provinces (cool-temperate, warm-temperate and subtropical). The caridean shrimp Palaemon peringueyi also occurs in all threeprovinces, but the fact that it can disperse both actively and passively (i.e. larval drifting, adult walking/swimming and potential adult rafting by means of floating objects) suggests that the amount of gene flow between regions may be too high for evolutionary divergence to have taken place. Samples of P. peringueyi were collected throughout South Africa and an intraspecific phylogeny was reconstructed using mitochondrial COI and 16S rRNA sequences. Three major clades were recovered, which were broadly associated with the three biogeographic regions. This suggests that, even though P. peringueyi can disperse actively, the fact that neither larvae nor adults are strong swimmers has resulted in genetic subdivisons comparable to those of passively dispersing coastal invertebrates in southern Africa.

Can novel genetic analyses help to identify low-dispersal marine invasive species?

Genetic methods can be a powerful tool to resolve the native versus introduced status of populations whose taxonomy and biogeography are poorly understood. The genetic study of introduced species is presently dominated by analyses that identify signatures of recent colonization by means of summary statistics. Unfortunately, such approaches cannot be used in low-dispersal species, in which recently established populations originating from elsewhere in the species native range also experience periods of low population size because they are founded by few individuals. We tested whether coalescent-based molecular analyses that provide detailed information about demographic history supported the hypothesis that a sea squirt whose distribution is centered on Tasmania was recently introduced to mainland Australia and New Zealand through human activities. Methods comparing trends in population size (Bayesian Skyline Plots and Approximate Bayesian Computation) were no more informative than summary statistics, likely because of recent intra-Tasmanian dispersal. However, IMa2 estimates of divergence between putatively native and introduced populations provided information at a temporal scale suitable to differentiate between recent (potentially anthropogenic) introductions and ancient divergence, and indicated that all three non-Tasmanian populations were founded during the period of European settlement. While this approach can be affected by inaccurate molecular dating, it has considerable (albeit largely unexplored) potential to corroborate nongenetic information in species with limited dispersal capabilities.

Historical demography of southern African patellid limpets: congruence of population expansions, but not phylogeography

Global climatic oscillations have shaped the contemporary genetic structure of marine taxa in different ways. Previous demographic studies have indicated that various intertidal marine species display genetic signatures of demographic expansion that either pre- or postdate the Last Glacial Maximum. Such expansions and the ability of species to colonise new habitats will influence their genetic structure, but the link between scales of larval dispersal and the strength of phylogeographic structure is not always clear. We analysed a fragment of the mitochondrial COI gene of 11 sympatric species of intertidal southern African patellid limpets to investigate how ancient oceanographic dynamics have shaped and maintained their contemporary spatial genetic variation. Our data show that the patellid limpets investigated display congruent evidence of spatial expansion during the Late Pleistocene or Early Holocene, which corresponds with the establishment of the contemporary southern African shoreline. We argue that closely related and co-distributed southern African intertidal invertebrates responded to ancient climatic oscillations as a cohesive group. In contrast, contemporary oceanographic circulation has shaped the phylogeographic patterns of these limpets in different ways. We show close relationships between phylogeography and biogeography for some species, but not for others, despite the similarities in their life histories and exposure to the same climatic changes.

Range-wide fragmentation in a threatened fish associated with post-European settlement modification in the Murray–Darling Basin, Australia

Distinguishing the relative influence of historic (i.e. natural) versus anthropogenic factors in metapopulation structure is an important but often overlooked step in management programs of threatened species. Biotas in freshwater wetlands and floodplains, such as those in the Murray–Darling Basin (MDB)—one of Australia’s most impacted ecosystems, are particularly susceptible to anthropogenic fragmentation. Here we present a comprehensive multilocus assessment of genetic variation in the threatened southern pygmy perch Nannoperca australis (578 individuals; 45 localities; microsatellite, allozyme and mitochondrial DNA datasets), an ecological specialist with low dispersal potential. We assess patterns of spatial structure and genetic diversity in populations spanning the highly fragmented MDB and test whether recent anthropogenic modification has disrupted range-wide connectivity. We detected strong and hierarchical population structure, very low genetic diversity and lack of contemporary gene flow across the MDB. In contrast, the apparent absence of pronounced or long-term phylogeographic structure suggests that observed population divergences generally do not reflect deeply historic natural fragmentation. Coalescent-based analyses supported this inference, revealing that divergence times between populations from the upper and lower MDB fall into the period of European settlement. It appears that the observed contemporary isolation of populations is partly explained by the severe modification of the MDB post-dating the onset of European settlement. Our integrated approach substantially improves the interpretation of how fragmentation impacts present-day biodiversity. It also provides novel contributions for risk-assessing management actions in the context of captive breeding and translocations of small freshwater fishes, a group of increasing global conservation concern.

Larval development reflects biogeography in two formerly synonymised southern African coastal crabs

The southern African crab Hymenosoma orbiculare was recently split into five distinct species, of which three are estuarine/coastal and have peripatric distributions that are linked to temperature-defined marine bioregions. This suggests that the species’ ranges may be limited by physiological adaptations to their thermal environment. We explored this hypothesis by rearing the larvae of the warm-temperate lineage of H. orbiculare and the warm-temperate/subtropical H. longicrure at a range of water temperatures, and found clear temperature-dependent differences in the duration of larval development. Our study contributes to the growing body of evidence that stresses the importance of adaptation to regional environmental conditions, rather than physical dispersal barriers on their own, in limiting the mixing of marine species between temperature-defined biogeographic regions.

Low genetic diversity in pygmy blue whales is due to climate-induced diversification rather than anthropogenic impacts

Unusually low genetic diversity can be a warning of an urgent need to mitigate causative anthropogenic activities. However, current low levels of genetic diversity in a population could also be due to natural historical events, including recent evolutionary divergence, or long-term persistence at a small population size. Here, we determine whether the relatively low genetic diversity of pygmy blue whales (Balaenoptera musculus brevicauda) in Australia is due to natural causes or overexploitation. We apply recently developed analytical approaches in the largest genetic dataset ever compiled to study blue whales (297 samples collected after whaling and representing lineages from Australia, Antarctica and Chile). We find that low levels of genetic diversity in Australia are due to a natural founder event from Antarctic blue whales (Balaenoptera musculus intermedia) that occurred around the Last Glacial Maximum, followed by evolutionary divergence. Historical climate change has therefore driven the evolution of blue whales into genetically, phenotypically and behaviourally distinct lineages that will likely be influenced by future climate change.

No divergent evolution, despite restricted connectivity, between Atlantic and Indian Ocean goby populations

Southern Africa is a marine biodiversity hotspot that not only comprises faunal elements from the Atlantic and Indian Oceans, but also large numbers of endemic species. Using mitochondrial and nuclear DNA sequence data, we explored whether genetic structure in the endemic coastal goby Psammogobius knysnaensis, a species whose range straddles both biomes, is linked to the boundary between the two oceans. Subtle genetic structure was identified between Atlantic and Indian Ocean populations, with genetic diversity being lower in the Atlantic, and particularly on the west coast. Our results point to partial isolation between the populations associated with each biome that is most likely driven by the region’s oceanography, but unlike in other species, there is no evidence for distinct regional evolutionary lineages that are likely adapted to the environmental conditions prevalent in each region. The exclusive presence of P. knysnaensis in sheltered habitats (estuaries and lagoons) may protect this species from the severe impacts of cold water upwelling on the west coast.

A comparison of genetic structure in two low-dispersal crabs from the Wild Coast, South Africa

The Wild Coast in south-eastern South Africa is strongly influenced by the warm, southward-flowing Agulhas Current. This current has a significant impact on dispersal in the coastal biota of the region, and facilitates high levels of connectivity among populations. However, it is not known how the regions high-velocity hydrology affects genetic population structure in endemic estuarine species, populations of which are frequently isolated from the sea. Here, we compared genetic structure in two estuarine crabs of the family Hymenosomatidae. Both are presumed to have low dispersal potential, but they differ in terms of their life histories. Hymenosoma longicrure has abbreviated larval development and can complete its entire life cycle within estuaries, whereas Neorhynchoplax bovis is a direct developer that lacks planktonic larvae. Using DNA sequence data from the mitochondrial COI gene and the intron of the nuclear ANT gene, we found that levels of genetic structure differ considerably between the species. Depending on the genetic marker used, H. longicrure is genetically homogeneous (COI) or displays low levels of genetic structure and minor evidence of recruitment near natal sites (ANT). In contrast, connectivity in N. bovis is much lower, as this species has a unique combination of alleles at each site, indicating that recruitment is mostly local. These results support previous findings suggesting that even a short larval dispersal phase is sufficient to maintain high levels of connectivity and prevent genetic divergence among populations.

Diversification and coevolution of the ghrelin/growth hormone secretagogue receptor system in vertebrates

Abstract The gut hormone ghrelin is involved in numerous metabolic functions, such as the stimulation of growth hormone secretion, gastric motility, and food intake. Ghrelin is modified by ghrelin O‐acyltransferase (GOAT) or membrane‐bound O‐acyltransferase domain‐containing 4 (MBOAT4) enabling action through the growth hormone secretagogue receptors (GHS‐R). During the course of evolution, initially strong ligand/receptor specificities can be disrupted by genomic changes, potentially modifying physiological roles of the ligand/receptor system. Here, we investigated the coevolution of ghrelin, GOAT, and GHS‐R in vertebrates. We combined similarity search, conserved synteny analyses, phylogenetic reconstructions, and protein structure comparisons to reconstruct the evolutionary history of the ghrelin system. Ghrelin remained a single‐gene locus in all vertebrate species, and accordingly, a single GHS‐R isoform was identified in all tetrapods. Similar patterns of the nonsynonymous (dN) and synonymous (dS) ratio (dN/dS) in the vertebrate lineage strongly suggest coevolution of the ghrelin and GHS‐R genes, supporting specific functional interactions and common physiological pathways. The selection profiles do not allow confirmation as to whether ghrelin binds specifically to GOAT, but the ghrelin dN/dS patterns are more similar to those of GOAT compared to MBOAT1 and MBOAT2 isoforms. Four GHS‐R isoforms were identified in teleost genomes. This diversification of GHS‐R resulted from successive rounds of duplications, some of which remained specific to the teleost lineage. Coevolution signals are lost in teleosts, presumably due to the diversification of GHS‐R but not the ghrelin gene. The identification of the GHS‐R diversity in teleosts provides a molecular basis for comparative studies on ghrelins physiological roles and regulation, while the comparative sequence and structure analyses will assist translational medicine to determine structure–function relationships of the ghrelin/GHS‐R system.

Mitochondrial DNA is unsuitable to test for isolation by distance

Tests for isolation by distance (IBD) are the most commonly used method of assessing spatial genetic structure. Many studies have exclusively used mitochondrial DNA (mtDNA) sequences to test for IBD, but this marker is often in conflict with multilocus markers. Here, we report a review of the literature on IBD, with the aims of determining (a) whether significant IBD is primarily a result of lumping spatially discrete populations, and (b) whether microsatellite datasets are more likely to detect IBD when mtDNA does not. We also provide empirical data from four species in which mtDNA failed to detect IBD by comparing these with microsatellite and SNP data. Our results confirm that IBD is mostly found when distinct regional populations are pooled, and this trend disappears when each is analysed separately. Discrepancies between markers were found in almost half of the studies reviewed, and microsatellites were more likely to detect IBD when mtDNA did not. Our empirical data rejected the lack of IBD in the four species studied, and support for IBD was particularly strong for the SNP data. We conclude that mtDNA sequence data are often not suitable to test for IBD, and can be misleading about species’ true dispersal potential. The observed failure of mtDNA to reliably detect IBD, in addition to being a single-locus marker, is likely a result of a selection-driven reduction in genetic diversity obscuring spatial genetic differentiation.