Thomas G. Dahlgren

Power for detecting genetic divergence: differences between statistical methods and marker loci

Information on statistical power is critical when planning investigations and evaluating empirical data, but actual power estimates are rarely presented in population genetic studies. We used computer simulations to assess and evaluate power when testing for genetic differentiation at multiple loci through combining test statistics or P values obtained by four different statistical approaches, viz. Pearsons chi‐square, the log‐likelihood ratio G‐test, Fishers exact test, and an FST‐based permutation test. Factors considered in the comparisons include the number of samples, their size, and the number and type of genetic marker loci. It is shown that power for detecting divergence may be substantial for frequently used sample sizes and sets of markers, also at quite low levels of differentiation. The choice of statistical method may be critical, though. For multi‐allelic loci such as microsatellites, combining exact P values using Fishers method is robust and generally provides a high resolving power. In contrast, for few‐allele loci (e.g. allozymes and single nucleotide polymorphisms) and when making pairwise sample comparisons, this approach may yield a remarkably low power. In such situations chi‐square typically represents a better alternative. The G‐test without Williamss correction frequently tends to provide an unduly high proportion of false significances, and results from this test should be interpreted with great care. Our results are not confined to population genetic analyses but applicable to contingency testing in general.

Biocomplexity in a highly migratory pelagic marine fish, Atlantic herring

The existence of biologically differentiated populations has been credited with a major role in conferring sustainability and in buffering overall productivity of anadromous fish population complexes where evidence for spatial structure is uncontroversial. Here, we describe evidence of correlated genetic and life history (spawning season linked to spawning location) differentiation in an abundant and highly migratory pelagic fish, Atlantic herring, Clupea harengus, in the North Sea (NS) and adjacent areas. The existence of genetically and phenotypically diverse stocks in this region despite intense seasonal mixing strongly implicates natal homing in this species. Based on information from genetic markers and otolith morphology, we estimate the proportional contribution by NS, Skagerrak (SKG) and Kattegat and western Baltic (WBS) fish to mixed aggregations targeted by the NS fishery. We use these estimates to identify spatial and temporal differences in life history (migratory behaviour) and habitat use among genetically differentiated migratory populations that mix seasonally. Our study suggests the existence of more complex patterns of intraspecific diversity than was previously recognized. Sustainability may be compromised if such complex patterns are reduced through generalized management (e.g. area closures) that overlooks population differences in spatial use throughout the life cycle.

Environmental correlates of population differentiation in Atlantic herring

Abstract The marine environment is characterized by few physical barries, and pelagic fishes commonly show high migratory potential and low, albeit in some cases statistically significant, levels of genetic divergence in neutral genetic marker analyses. however, it is not clear whether low levels of differentiation reflect spactially separated populations experiencing gene flow or shallow population histories coupled with limited random genetic drift in large, demographically isolated populations undergoing independent evlolutionary processes. using information for nine microsatellite loci in a total of 1951 fish, we analyzed genetic differentiation among Atlantic herring from eleven spawning locations distributed along a longitudinal aradient from the North Sea to the Western Baltic. Overall genetic differentiation was low (θ=0.008) but statistically significant. The area is characterized by a dramatic shift in hydrography from the highly saline and temperature stable North Sea to the brackish Baltic Sea, where temperatures show high annual variation. We used two different methods, a novel computational geometric approach and partial Mantel correlation analysis coupled with detailed environmental information form spawning locations to show that patterns of reproductive isolation covaried with salinity differences among spawning locations, independent of their geographical distance. We show that reproductive isolation can be maintained in marine fish populations exhibiting substantial mixing during larval and adult life stages. Analyses incorporating genetic, spatial, and environmental parameters indicated that isolation mechanisms are associated with the specific salinity conditions on spawning locations.

World-wide whale worms? A new species of Osedax from the shallow north Atlantic

We describe a new species of the remarkable whalebone-eating siboglinid worm genus, Osedax, from a whale carcass in the shallow north Atlantic, west of Sweden. Previously only recorded from deep-sea (1500–3000 m) whale-falls in the northeast Pacific, this is the first species of Osedax known from a shelf-depth whale-fall, and the first from the Atlantic Ocean. The new species, Osedax mucofloris sp. n., is abundant on the bones of an experimentally implanted Minke whale carcass (Balaenoptera acutorostrata) at 125 m depth in the shallow North Sea. O. mucofloris can be cultured on bones maintained in aquaria. The presence of O. mucofloris in the shallow North Sea and northeast Pacific suggests global distribution on whale-falls for the Osedax clade. Molecular evidence from mitochondrial cytochrome oxidase 1 (CO1) and 18S rRNA sequences suggests that O. mucofloris has high dispersal rates, and provides support for the idea of whale-falls acting as ‘stepping-stones’ for the global dispersal of siboglinid annelids over ecological and evolutionary time.

Detecting population structure in a high gene-flow species, Atlantic herring (Clupea harengus): direct, simultaneous evaluation of neutral vs putatively selected loci.

In many marine fish species, genetic population structure is typically weak because populations are large, evolutionarily young and have a high potential for gene flow. We tested whether genetic markers influenced by natural selection are more efficient than the presumed neutral genetic markers to detect population structure in Atlantic herring (Clupea harengus), a migratory pelagic species with large effective population sizes. We compared the spatial and temporal patterns of divergence and statistical power of three traditional genetic marker types, microsatellites, allozymes and mitochondrial DNA, with one microsatellite locus, Cpa112, previously shown to be influenced by divergent selection associated with salinity, and one locus located in the major histocompatibility complex class IIA (MHC-IIA) gene, using the same individuals across analyses. Samples were collected in 2002 and 2003 at two locations in the North Sea, one location in the Skagerrak and one location in the low-saline Baltic Sea. Levels of divergence for putatively neutral markers were generally low, with the exception of single outlier locus/sample combinations; microsatellites were the most statistically powerful markers under neutral expectations. We found no evidence of selection acting on the MHC locus. Cpa112, however, was highly divergent in the Baltic samples. Simulations addressing the statistical power for detecting population divergence showed that when using Cpa112 alone, compared with using eight presumed neutral microsatellite loci, sample sizes could be reduced by up to a tenth while still retaining high statistical power. Our results show that the loci influenced by selection can serve as powerful markers for detecting population structure in high gene-flow marine fish species.

New perspectives on the ecology and evolution of siboglinid tubeworms

Siboglinids are tube-dweling annelids that are important members of deep-sea chemosynthetic communities, which include hydrothermal vents, cold seeps, whale falls and reduced sediments. As adults, they lack a functional digestive system and rely on microbial endosymbionts for their energetic needs. Recent years have seen a revolution in our understanding of these fascinating worms. Molecular systematic methods now place these animals, formerly known as the phyla Pogonophora and Vestimentifera, within the polychaete clade Siboglinidae. Furthermore, an entirely new radiation of siboglinids, Osedax, has just recently been discovered living on whale bones. The unique and intricate evolutionary association of siboglinids with both geology, in the formation of spreading centres and seeps, and biology with the evolution of large whales, offers opportunities for studies of vicariant evolution and the calibration of molecular clocks. Moreover, new advances in our knowledge of siboglinid anatomy coupled with molecular characterization of microbial symbiont communities are revolutionizing our knowledge of host-symbiont relationships in the Metazoa. Despite these advances, considerable debate persists concerning the evolutionary history of siboglinids. Here we review the morphological, molecular, ecological and fossil data in order to address when and how siboglinids evolved. We discuss the role of ecological conditions in the evolution of siboglinids and present possible scenarios of the evolutionary origin of the symbiotic relationships between siboglinids and their endosymbiotic bacteria.

Position and Delineation of Chrysopetalidae and Hesionidae (Annelida, Polychaeta, Phyllodocida)

Previous studies suggest that the polychaete taxa Hesionidae and Chrysopetalidae may not represent separate groups, that Pilargidae constitute a subgroup within Hesionidae, and that Hesionides and Microphthalmus are highly derived hesionids. Phylogenetic systematic analyses of Phyllodocida and the subgroup Nereidiformia are presented in order to clarify the position and delineation of these taxa. The phyllodocida analysis includes 18 families representing the majority of the taxa in the group, is rooted with Onuphidae, and is based on 42 absent/present coded morphological characters, obtained mainly from literature. All 69 resulting shortest trees include the clade (Chrysopetalidae, Nereididae, Hesionidae), but with either Syllidae, Nautiliniellidae, Pilargidae or (Aphroditiformia, Pisionidae) as sister. In‐ and outgroup taxon selection for the Nereidiformia study is dictated by the outcome of Phyllodocida analysis, with scores based on examined species of two chrysopetalids, four hesionids, one nereid, one pilargid, one pisionid, one syllid, plus the putative hesionids Hesionides arenaria and Microphthalmus sp. It is based on 46 absent/present coded morphological characters. Two equally parsimonious trees indicate that chrysopetalids and hesionids are well delineated, that pilargids and hesionids are non‐overlapping, and that Microphthalmus and Hesionides are not hesionids.

Temporally stable genetic structure of heavily exploited Atlantic herring (Clupea harengus) in Swedish waters.

Information on the temporal stability of genetic structures is important to permit detection of changes that can constitute threats to biological resources. Large-scale harvesting operations are known to potentially alter the composition and reduce the variability of populations, and Atlantic herring (Clupea harengus) has a long history of heavy exploitation. In the Baltic Sea and Skagerrak waters, the census population sizes have declined by 35–50% over the last three decades. We compared the genetic structure of Atlantic herring in these waters sampled at least two different times between 1979 and 2003 by assaying 11 allozyme and nine microsatellite loci. We cannot detect any changes in the amount of genetic variation or spatial structure, and differentiation is weak with overall FST=0.003 among localities for the older samples and FST=0.002 for the newer ones. There are indications of temporal allele frequency changes, particularly in one of five sampling localities that is reflected in a relatively small local Ne estimate of c. 400. The previously identified influence of selection at the microsatellite locus Cpa112 remains stable over the 24-year period studied here. Despite little genetic differentiation, migration among localities appears small enough to permit demographic independence between populations.

Molecular Phylogeny of the Model Annelid Ophryotrocha

Annelids of the genus Ophryotrocha are small opportunistic worms commonly found in polluted and nutrient-rich habitats such as harbors. Within this small group of about 40 described taxa a large variety of reproductive strategies are found, ranging from gonochoristic broadcast spawners to sequential hermaphroditic brooders. Many of the species have a short generation time and are easily maintained as laboratory cultures. Thus they have become a popular system for exploring a variety of biological questions including developmental genetics, ethology, and sexual selection. Despite considerable behavioral, reproductive, and karyological studies, a phylogenetic framework is lacking because most taxa are morphologically similar. In this study we use 16S mitochondrial gene sequence data to infer the phylogeny of Ophryotrocha strains commonly used in the laboratory. The resulting mtDNA topologies are generally well resolved and support a genetic split between hermaphroditic and gonochoristic species. Although the ancestral state could not be unambiguously identified, a change in reproductive strategy (i.e., hermaphroditism and gonochorism) occurred once within Ophryotrocha. Additionally, we show that sequential hermaphroditism evolved from a simultaneous hermaphroditic ancestor, and that characters previously used in phylogenetic reconstruction (i.e., jaw morphology and shape of egg mass) are homoplasic within the group.

Unsegmented Annelids? Possible Origins of Four Lophotrochozoan Worm Taxa

Abstract In traditional classification schemes, the Annelida consists of the Polychaeta and the Clitellata (the latter including the Oligochaeta and Hirudinida). However, recent analyses suggest that annelids are much more diverse than traditionally believed, and that polychaetes are paraphyletic. Specifically, some lesser-known taxa (previously regarded as separate phyla) appear to fall within the annelid radiation. Abundant molecular, developmental, and morphological data show that the Siboglinidae, which includes the formerly recognized Pogonophora and Vestimentifera, are derived annelids; recent data from the Elongation Factor-1α (EF-1α) gene also suggest that echiurids are of annelid ancestry. Further, the phylogenetic origins of two other lesser-known groups of marine worms, the Myzostomida and Sipuncula, have recently been called into question. Whereas some authors advocate annelid affinities, others argue that these taxa do not fall within the annelid radiation. With advances in our understanding of annelid phylogeny, our perceptions of body plan evolution within the Metazoa are changing. The evolution of segmentation probably is more plastic than traditionally believed. However, as our understanding of organismal evolution is being revised, we are also forced to reconsider the specific characters being examined. Should segmentation be considered a developmental process or an ontological endpoint?