Publications by authors named "Daniel E Ruzzante"

53 Publications

Chromosome level reference of Atlantic halibut Hippoglossus hippoglossus provides insight into the evolution of sexual determination systems.

Mol Ecol Resour 2021 Mar 2. Epub 2021 Mar 2.

Biology Department, Dalhousie University, Halifax, NS, Canada.

Changes in the genetic mechanisms that control sexual determination have occurred independently across the tree of life, and with exceptional frequency in teleost fishes. To investigate the genomic changes underlying the evolution of sexual determination, we sequenced a chromosome-level genome, multitissue transcriptomes, and reduced representation population data for the Atlantic halibut (Hippoglossus hippoglossus), which has an XY/XX sex determination mechanism and has recently diverged (0.9-3.8 Ma) from the Pacific halibut (Hippoglossus stenolepis), which has a ZZ/ZW system. We used frequency and coverage-based population approaches to identify a putative sex-determining factor, GSDF. We characterized regions with elevated heterozygosity and linkage disequilibrium indicating suppression of recombination across a nascent sex chromosome. We detected testis-specific expression of GSDF, the sequence of which is highly conserved across flatfishes. Based on evidence from genome-wide association, coverage, linkage disequilibrium, testis and brain transcriptomes, and sequence conservation with other flatfishes, we propose a mechanism for the recent evolution of an XY sex-determination mechanism in Atlantic halibut. Changes to the ancestral sex-determining gene DMRT1 in regulating the downstream gene GSDF probably coincided with GSDF, or a proximal regulatory element of it, becoming the primary sex-determining factor. Our results suggest changes to a small number of elements can have drastic repercussions for the genomic substrate available to sex-specific evolutionary forces, providing insight into how certain elements repeatedly evolve to control sex across taxa. Our chromosome-level assembly, multitissue transcriptomes, and population genomic data provide a valuable resource and understanding of the evolution of sexual systems in fishes.
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http://dx.doi.org/10.1111/1755-0998.13369DOI Listing
March 2021

Functional genetic diversity in an exploited marine species and its relevance to fisheries management.

Proc Biol Sci 2021 Feb 24;288(1945):20202398. Epub 2021 Feb 24.

School of Aquatic and Fishery Sciences, University of Washington, 1122 NE Boat Street, Seattle WA 98105, USA.

The timing of reproduction influences key evolutionary and ecological processes in wild populations. Variation in reproductive timing may be an especially important evolutionary driver in the marine environment, where the high mobility of many species and few physical barriers to migration provide limited opportunities for spatial divergence to arise. Using genomic data collected from spawning aggregations of Pacific herring () across 1600 km of coastline, we show that reproductive timing drives population structure in these pelagic fish. Within a specific spawning season, we observed isolation by distance, indicating that gene flow is also geographically limited over our study area. These results emphasize the importance of considering both seasonal and spatial variation in spawning when delineating management units for herring. On several chromosomes, we detected linkage disequilibrium extending over multiple Mb, suggesting the presence of chromosomal rearrangements. Spawning phenology was highly correlated with polymorphisms in several genes, in particular , which influences the development of retinal photoreceptors in vertebrates. is probably within a chromosomal rearrangement in Pacific herring and is also associated with spawn timing in Atlantic herring (). The observed genetic diversity probably underlies resource waves provided by spawning herring. Given the ecological, economic and cultural significance of herring, our results support that conserving intraspecific genetic diversity is important for maintaining current and future ecosystem processes.
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http://dx.doi.org/10.1098/rspb.2020.2398DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7934995PMC
February 2021

Investigating Diadromy in Fishes and Its Loss in an -Omics Era.

iScience 2020 Dec 20;23(12):101837. Epub 2020 Nov 20.

Department of Biology, Dalhousie University, Halifax, Nova Scotia, B3H 4R2, Canada.

Diadromy, the predictable movements of individuals between marine and freshwater environments, is biogeographically and phylogenetically widespread across fishes. Thus, despite the high energetic and potential fitness costs involved in moving between distinct environments, diadromy appears to be an effective life history strategy. Yet, the origin and molecular mechanisms that underpin this migratory behavior are not fully understood. In this review, we aim first to summarize what is known about diadromy in fishes; this includes the phylogenetic relationship among diadromous species, a description of the main hypotheses regarding its origin, and a discussion of the presence of non-migratory populations within diadromous species. Second, we discuss how recent research based on -omics approaches (chiefly genomics, transcriptomics, and epigenomics) is beginning to provide answers to questions on the genetic bases and origin(s) of diadromy. Finally, we suggest future directions for -omics research that can help tackle questions on the evolution of diadromy.
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http://dx.doi.org/10.1016/j.isci.2020.101837DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7718486PMC
December 2020

Genomic basis of the loss of diadromy in Galaxias maculatus: Insights from reciprocal transplant experiments.

Mol Ecol 2020 12 4;29(24):4857-4870. Epub 2020 Nov 4.

Department of Biology, Dalhousie University, Halifax, NS, Canada.

Diadromy is known for having major effects on the distribution and richness of aquatic species, and so does its loss. The loss of diadromy has led to the diversification of many species, yet research focusing on understanding its molecular basis and consequences are limited. This is particularly true for amphidromous species despite being the most abundant group of diadromous species. Galaxias maculatus, an amphidromous species and one of the most widely distributed fishes in the Southern Hemisphere, exhibits many instances of nonmigratory or resident populations. The existence of naturally replicated resident populations in Patagonia can serve as an ideal system for the study of the mechanisms that lead to the loss of the diadromy and its ecological and evolutionary consequences. Here, we studied two adjacent river systems in which resident populations are genetically differentiated yet derived from the same diadromous population. By combining a reciprocal transplant experiment with genomic data, we showed that the two resident populations followed different evolutionary pathways by exhibiting a differential response in their capacity to survive in salt water. While one resident population was able to survive salt water, the other was not. Genomic analyses provided insights into the genes that distinguished (a) migratory from nonmigratory populations; (b) populations that can vs those that cannot survive a saltwater environment; and (c) between these resident populations. This study demonstrates that the loss of diadromy can be achieved by different pathways and that environmental (selection) and random (genetic drift) forces shape this dynamic evolutionary process.
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http://dx.doi.org/10.1111/mec.15686DOI Listing
December 2020

Limited genetic parallelism underlies recent, repeated incipient speciation in geographically proximate populations of an Arctic fish (Salvelinus alpinus).

Mol Ecol 2020 11 3;29(22):4280-4294. Epub 2020 Oct 3.

Department of Biology, Dalhousie University, Halifax, NS, Canada.

The genetic underpinnings of incipient speciation, including the genomic mechanisms which contribute to morphological and ecological differentiation and reproductive isolation, remain poorly understood. The repeated evolution of consistently, phenotypically distinct morphs of Arctic Charr (Salvelinus alpinus) within the Quaternary period offer an ideal model to study the repeatability of evolution at the genomic level. Sympatric morphs of Arctic Charr are found across this species' circumpolar distribution. However, the specific genetic mechanisms driving this morph differentiation are largely unknown despite the cultural and economic importance of the anadromous morph. We used a newly designed 87k SNP chip to investigate the character and consistency of the genomic differences among sympatric morphs within three recently deglaciated and geographically proximate lakes in Labrador, Canada. We found genetically distinct small and large morph Arctic Charr in all three lakes consistent with resident and anadromous morphs, respectively. A degree of reproductive isolation among sympatric morphs is likely given genome-wide distributions of outlier SNPs and high genome-wide F s. Across all lakes, outlier SNPs were largely nonoverlapping suggesting a lack of genetic parallelism driving morph differentiation. Alternatively, several genes and paralogous copies of the same gene consistently differentiated morphs across multiple lakes suggesting their importance to the manifestation of morphs. Our results confirm the utility of Arctic Charr as a model for investigating the predictability of evolution and support the importance of both genetic parallelism and nonparallelism to the incipient speciation of Arctic Charr morphs.
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http://dx.doi.org/10.1111/mec.15634DOI Listing
November 2020

Multiple drainage reversal episodes and glacial refugia in a Patagonian fish revealed by sequenced microsatellites.

Proc Biol Sci 2020 06 3;287(1928):20200468. Epub 2020 Jun 3.

Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada.

The rise of the southern Andes and the Quaternary glacial cycles influenced the landscape of Patagonia, affecting the phylogeographic and biogeographic patterns of its flora and fauna. Here, we examine the phylogeography of the freshwater fish, using 53 sequenced microsatellite DNA markers Fish ( 835) were collected from 16 river systems (46 locations) spanning the species range on both sides of the Andes. Eleven watersheds drain to the Pacific, five of which are trans-Andean (headwaters east of Andes). The remaining five drainages empty into the Atlantic. Three analytical approaches (neighbour-joining tree, hierarchical AMOVAs, Structure) revealed evidence of historic drainage reversals: fish from four of the five trans-Andean systems (Puelo, Futalaufquen/Yelcho, Baker, Pascua) exhibited greater genetic similarity with Atlantic draining systems than with Pacific systems with headwaters west of Andes. Present-day drainage (Pacific versus Atlantic) explained only 5% of total genetic variance, while ancestral drainage explained nearly 27% of total variance. Thus, the phylogeographic structure of is consistent with episodes of drainage reversal in multiple systems and suggests a major role for deglaciation in the genetic and indeed the geographical distribution of in Patagonia. The study emphasizes the significant role of historical processes in the current pattern of genetic diversity and differentiation in a fish from a southern temperate region.
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http://dx.doi.org/10.1098/rspb.2020.0468DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7341911PMC
June 2020

Resolving fine-scale population structure and fishery exploitation using sequenced microsatellites in a northern fish.

Evol Appl 2020 May 20;13(5):1055-1068. Epub 2020 Feb 20.

Department of Ocean Sciences Memorial University of Newfoundland St. John's NL Canada.

The resiliency of populations and species to environmental change is dependent on the maintenance of genetic diversity, and as such, quantifying diversity is central to combating ongoing widespread reductions in biodiversity. With the advent of next-generation sequencing, several methods now exist for resolving fine-scale population structure, but the comparative performance of these methods for genetic assignment has rarely been tested. Here, we evaluate the performance of sequenced microsatellites and a single nucleotide polymorphism (SNP) array to resolve fine-scale population structure in a critically important salmonid in north eastern Canada, Arctic Charr (). We also assess the utility of sequenced microsatellites for fisheries applications by quantifying the spatial scales of movement and exploitation through genetic assignment of fishery samples to rivers of origin and comparing these results with a 29-year tagging dataset. Self-assignment and simulation-based analyses of 111 genome-wide microsatellite loci and 500 informative SNPs from 28 populations of Arctic Charr in north-eastern Canada identified largely river-specific genetic structure. Despite large differences (~4X) in the number of loci surveyed between panels, mean self-assignment accuracy was similar with the microsatellite loci and the SNP panel (>90%). Subsequent analysis of 996 fishery-collected samples using the microsatellite panel revealed that larger rivers contribute greater numbers of individuals to the fishery and that coastal fisheries largely exploit individuals originating from nearby rivers, corroborating results from traditional tagging experiments. Our results demonstrate the efficacy of sequence-based microsatellite genotyping to advance understanding of fine-scale population structure and harvest composition in northern and understudied species.
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http://dx.doi.org/10.1111/eva.12922DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7232759PMC
May 2020

Human-induced habitat fragmentation effects on connectivity, diversity, and population persistence of an endemic fish, , in the Biobío River basin (Chile).

Evol Appl 2020 Apr 9;13(4):794-807. Epub 2019 Dec 9.

Department of Biology Dalhousie University Halifax NS Canada.

An understanding of how genetic variability is distributed in space is fundamental for the conservation and maintenance of diversity in spatially fragmented and vulnerable populations. While fragmentation can occur from natural barriers, it can also be exacerbated by anthropogenic activities such as hydroelectric power plant development. Whatever the source, fragmentation can have significant ecological effects, including disruptions of migratory processes and gene flow among populations. In Chile, the Biobío River basin exhibits a high degree of habitat fragmentation due to the numerous hydroelectric power plants in operation, the number of which is expected to increase following new renewable energy use strategies. Here, we assessed the effects of different kinds of barriers on the genetic structure of the endemic freshwater fish , knowledge that is critically needed to inform conservation strategies in light of current and anticipated further fragmentation initiatives in the system. We identified eight genetic units throughout the entire Biobío system with high effective sizes. A reduced effective size estimate was, however, observed in a single population located between two impassable barriers. Both natural waterfalls and human-made dams were important drivers of population differentiation in this system; however, dams affect genetic diversity differentially depending on their mode of operation. Evidence of population extirpation was found in two river stretches limited by upstream and downstream dams. Significant gene flow in both directions was found among populations not separated by natural or anthropogenic barriers. Our results suggest a significant vulnerability of populations to future dam development and demonstrate the importance of studying basin-wide data sets with genetic metrics to understand the strength and direction of anthropogenic impacts on fish populations.
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http://dx.doi.org/10.1111/eva.12901DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7086057PMC
April 2020

The effects of diadromy and its loss on genomic divergence: The case of amphidromous Galaxias maculatus populations.

Mol Ecol 2019 12 17;28(24):5217-5231. Epub 2019 Nov 17.

Department of Biology, Dalhousie University, Halifax, Canada.

Understanding the evolutionary mechanisms that affect the genetic divergence between diadromous and resident populations across heterogeneous environments is a challenging task. While diadromy may promote gene flow leading to a lack of genetic differentiation among populations, resident populations tend to be affected by local adaptation and/or plasticity. Studies on these effects on genomic divergence in nonmodel amphidromous species are scarce. Galaxias maculatus, one of the most widespread fish species in the Southern Hemisphere, exhibits two life histories, an ancestral diadromous, specifically, amphidromous form, and a derived freshwater resident form. We examined the genetic diversity and divergence among 20 estuarine and resident populations across the Chilean distribution of G. maculatus and assessed the extent to which selection is involved in the differentiation among resident populations. We obtained nearly 4,400 SNP markers using a RADcap approach for 224 individuals. As expected, collections from estuarine locations typically consist of diadromous individuals. Diadromous populations are highly differentiated from their resident counterparts by both neutral and putative adaptive markers. While diadromous populations exhibit high gene flow and lack site fidelity, resident populations appear to be the product of different colonization events with relatively low genetic diversity and varying levels of gene flow. In particular, the northernmost resident populations were clearly genetically distinct and reproductively isolated from each other suggesting local adaptation. Our study provides insights into the role of life history differences in the maintenance of genetic diversity and the importance of genetic divergence in species evolution.
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http://dx.doi.org/10.1111/mec.15290DOI Listing
December 2019

Invasive species and postglacial colonization: their effects on the genetic diversity of a Patagonian fish.

Proc Biol Sci 2019 02;286(1897):20182567

1 Department of Biology, Dalhousie University , 1355 Oxford Street, Halifax, Nova Scotia, Canada B3H 4R2.

The present distribution of Patagonian species is the result of a complex history involving Quaternary refugial populations, Holocene range expansions and demographic changes occurring during the Anthropocene. Invasive salmonids were introduced in Patagonia during the last century, occupying most rivers and lakes, preying on and competing with native species, including the fish Galaxias platei. Here, we used G. platei as a case study to understand how long-term (i.e. population differentiation during the Holocene) and short-term historical processes (salmonid introductions) affect genetic diversity. Using a suite of microsatellite markers, we found that the number of alleles is negatively correlated with the presence of salmonids (short-term processes), with G. platei populations from lakes with salmonids exhibiting significantly lower genetic diversity than populations from lakes without salmonids. Simulations (100 years backwards) showed that this difference in genetic diversity can be explained by a 99% reduction in population size. Allelic richness and observed heterozygosities were also negatively correlated with the presence of salmonids, but also positively correlated with long-term processes linked to Quaternary glaciations. Our results show how different genetic parameters can help identify processes taking place at different scales and their importance in terms of conservation.
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http://dx.doi.org/10.1098/rspb.2018.2567DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6408905PMC
February 2019

Extensive secondary contact among three glacial lineages of Arctic Char () in Labrador and Newfoundland.

Ecol Evol 2019 Feb 28;9(4):2031-2045. Epub 2019 Jan 28.

Department of Biology Dalhousie University Halifax Nova Scotia Canada.

Aim: The Pleistocene glaciation event prompted the allopatric divergence of multiple glacial lineages of Arctic char (), some of which have come into secondary contact upon their recolonization of the Holarctic. While three glacial lineages (Arctic, Atlantic, and Acadian) are known to have recolonized the western Atlantic, the degree of overlap of these three lineages is largely unknown. We sought to determine the distribution of these three glacial lineages in Labrador and Newfoundland at a fine spatial scale to assess their potential for introgression and their relative contribution to local fisheries.

Location: Labrador and Newfoundland, Canada.

Methods: We sequenced a portion of the D-loop region in over 1,000 Arctic char () samples from 67 locations across Labrador and Newfoundland.

Results: Within Labrador, the Arctic and Atlantic lineages were widespread. Two locations (one landlocked and one with access to the sea) also contained individuals of the Acadian lineage, constituting the first record of this lineage in Labrador. Atlantic and Acadian lineage individuals were found in both eastern and western Newfoundland. Multiple sampling locations in Labrador and Newfoundland contained fish of two or more different glacial lineages, implying their introgression. Glacial lineage did not appear to dictate contemporary genetic divergence between the pale and dark morph of char present in Gander Lake, Newfoundland. Both were predominately of the Atlantic lineage, suggesting the potential for their divergence in sympatry.

Main Conclusions: Our study reveals Labrador and Newfoundland to be a unique junction of three glacial lineages which have likely hybridized extensively in this region.
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http://dx.doi.org/10.1002/ece3.4893DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6392391PMC
February 2019

Temporal stability and assignment power of adaptively divergent genomic regions between herring () seasonal spawning aggregations.

Ecol Evol 2019 Jan 11;9(1):500-510. Epub 2018 Dec 11.

Department of Biology Dalhousie University Halifax Nova Scotia Canada.

Atlantic herring (), a vital ecosystem component and target of the largest Northwest Atlantic pelagic fishery, undergo seasonal spawning migrations that result in elusive sympatric population structure. Herring spawn mostly in fall or spring, and genomic differentiation was recently detected between these groups. Here we used a subset of this differentiation, 66 single nucleotide polymorphisms (SNPs) to analyze the temporal dynamics of this local adaptation and the applicability of SNP subsets in stock assessment. We showed remarkable temporal stability of genomic differentiation corresponding to spawning season, between samples taken a decade apart (2005  = 90 vs. 2014  = 71) in the Gulf of St. Lawrence, and new evidence of limited interbreeding between spawning components. We also examined an understudied and overexploited herring population in Bras d'Or lake ( = 97); using highly reduced SNP panels ( > 6), we verified little-known sympatric spawning populations within this unique inland sea. These results describe consistent local adaptation, arising from asynchronous reproduction in a migratory and dynamic marine species. Our research demonstrates the efficiency and precision of SNP-based assessments of sympatric subpopulations; and indeed, this temporally stable local adaptation underlines the importance of such fine-scale management practices.
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http://dx.doi.org/10.1002/ece3.4768DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6342187PMC
January 2019

Past, present, and future of a freshwater fish metapopulation in a threatened landscape.

Conserv Biol 2018 08 18;32(4):849-859. Epub 2018 Apr 18.

Department of Biology, Dalhousie University, 1355 Oxford Street, Halifax, NS B3H 4R2, Canada.

It is well documented that hydropower plants can affect the dynamics of fish populations through landscape alterations and the creation of new barriers. Less emphasis has been placed on the examination of the genetic consequences for fish populations of the construction of dams. The relatively few studies that focus on genetics often do not consider colonization history and even fewer tend to use this information for conservation purposes. As a case study, we used a 3-pronged approach to study the influence of historical processes, contemporary landscape features, and potential future anthropogenic changes in landscape on the genetic diversity of a fish metapopulation. Our goal was to identify the metapopulation's main attributes, detect priority areas for conservation, and assess the consequences of the construction of hydropower plants for the persistence of the metapopulation. We used microsatellite markers and coalescent approaches to examine historical colonization processes, traditional population genetics, and simulations of future populations under alternate scenarios of population size reduction and gene flow. Historical gene flow appeared to have declined relatively recently and contemporary populations appeared highly susceptible to changes in landscape. Gene flow is critical for population persistence. We found that hydropower plants could lead to a rapid reduction in number of alleles and to population extirpation 50-80 years after their construction. More generally, our 3-pronged approach for the analyses of empirical genetic data can provide policy makers with information on the potential impacts of landscape changes and thus lead to more robust conservation efforts.
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http://dx.doi.org/10.1111/cobi.13093DOI Listing
August 2018

Whole-genome sequencing approaches for conservation biology: Advantages, limitations and practical recommendations.

Mol Ecol 2017 Oct 5;26(20):5369-5406. Epub 2017 Sep 5.

Department of Biology, Dalhousie University, Halifax, NS, Canada.

Whole-genome resequencing (WGR) is a powerful method for addressing fundamental evolutionary biology questions that have not been fully resolved using traditional methods. WGR includes four approaches: the sequencing of individuals to a high depth of coverage with either unresolved or resolved haplotypes, the sequencing of population genomes to a high depth by mixing equimolar amounts of unlabelled-individual DNA (Pool-seq) and the sequencing of multiple individuals from a population to a low depth (lcWGR). These techniques require the availability of a reference genome. This, along with the still high cost of shotgun sequencing and the large demand for computing resources and storage, has limited their implementation in nonmodel species with scarce genomic resources and in fields such as conservation biology. Our goal here is to describe the various WGR methods, their pros and cons and potential applications in conservation biology. WGR offers an unprecedented marker density and surveys a wide diversity of genetic variations not limited to single nucleotide polymorphisms (e.g., structural variants and mutations in regulatory elements), increasing their power for the detection of signatures of selection and local adaptation as well as for the identification of the genetic basis of phenotypic traits and diseases. Currently, though, no single WGR approach fulfils all requirements of conservation genetics, and each method has its own limitations and sources of potential bias. We discuss proposed ways to minimize such biases. We envision a not distant future where the analysis of whole genomes becomes a routine task in many nonmodel species and fields including conservation biology.
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http://dx.doi.org/10.1111/mec.14264DOI Listing
October 2017

Parallel adaptive evolution of geographically distant herring populations on both sides of the North Atlantic Ocean.

Proc Natl Acad Sci U S A 2017 04 7;114(17):E3452-E3461. Epub 2017 Apr 7.

Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, 752 36 Uppsala, Sweden;

Atlantic herring is an excellent species for studying the genetic basis of adaptation in geographically distant populations because of its characteristically large population sizes and low genetic drift. In this study we compared whole-genome resequencing data of Atlantic herring populations from both sides of the Atlantic Ocean. An important finding was the very low degree of genetic differentiation among geographically distant populations (fixation index = 0.026), suggesting lack of reproductive isolation across the ocean. This feature of the Atlantic herring facilitates the detection of genetic factors affecting adaptation because of the sharp contrast between loci showing genetic differentiation resulting from natural selection and the low background noise resulting from genetic drift. We show that genetic factors associated with timing of reproduction are shared between genetically distinct and geographically distant populations. The genes for thyroid-stimulating hormone receptor (), the SOX11 transcription factor (), calmodulin (), and estrogen receptor 2 (), all with a significant role in reproductive biology, were among the loci that showed the most consistent association with spawning time throughout the species range. In fact, the same two SNPs located at the 5' end of showed the most significant association with spawning time in both the east and west Atlantic. We also identified unexpected haplotype sharing between spring-spawning oceanic herring and autumn-spawning populations across the Atlantic Ocean and the Baltic Sea. The genomic regions showing this pattern are unlikely to control spawning time but may be involved in adaptation to ecological factor(s) shared among these populations.
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http://dx.doi.org/10.1073/pnas.1617728114DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5410801PMC
April 2017

A portrait of a sucker using landscape genetics: how colonization and life history undermine the idealized dendritic metapopulation.

Mol Ecol 2016 Sep 10;25(17):4126-45. Epub 2016 Aug 10.

Department of Biology, Dalhousie University, Halifax, NS, B3H4R2, Canada.

Dendritic metapopulations have been attributed unique properties by in silico studies, including an elevated genetic diversity relative to a panmictic population of equal total size. These predictions have not been rigorously tested in nature, nor has there been full consideration of the interacting effects among contemporary landscape features, colonization history and life history traits of the target species. We tested for the effects of dendritic structure as well as the relative importance of life history, environmental barriers and historical colonization on the neutral genetic structure of a longnose sucker (Catostomus catostomus) metapopulation in the Kogaluk watershed of northern Labrador, Canada. Samples were collected from eight lakes, genotyped with 17 microsatellites, and aged using opercula. Lakes varied in differentiation, historical and contemporary connectivity, and life history traits. Isolation by distance was detected only by removing two highly genetically differentiated lakes, suggesting a lack of migration-drift equilibrium and the lingering influence of historical factors on genetic structure. Bayesian analyses supported colonization via the Kogaluk's headwaters. The historical concentration of genetic diversity in headwaters inferred by this result was supported by high historical and contemporary effective sizes of the headwater lake, T-Bone. Alternatively, reduced allelic richness in headwaters confirmed the dendritic structure's influence on gene flow, but this did not translate to an elevated metapopulation effective size. A lack of equilibrium and upstream migration may have dampened the effects of dendritic structure. We suggest that interacting historical and contemporary factors prevent the achievement of the idealized traits of a dendritic metapopulation in nature.
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http://dx.doi.org/10.1111/mec.13757DOI Listing
September 2016

Scorched mussels (Brachidontes spp., Bivalvia: Mytilidae) from the tropical and warm-temperate southwestern Atlantic: the role of the Amazon River in their speciation.

Ecol Evol 2016 Mar 18;6(6):1778-98. Epub 2016 Feb 18.

Department of Biology Dalhousie University 1355 Oxford St. Halifax Nova Scotia B3H 4R2 Canada.

Antitropicality is a distribution pattern where closely related taxa are separated by an intertropical latitudinal gap. Two potential examples include Brachidontes darwinianus (south eastern Brazil to Uruguay), considered by some authors as a synonym of B. exustus (Gulf of Mexico and the Caribbean), and B. solisianus, distributed along the Brazilian coast with dubious records north of the intertropical zone. Using two nuclear (18S and 28S rDNA) and one mitochondrial gene (mtDNA COI), we aimed to elucidate the phylogeographic and phylogenetic relationships among the scorched mussels present in the warm-temperate region of the southwest Atlantic. We evaluated a divergence process mediated by the tropical zone over alternative phylogeographic hypotheses. Brachidontes solisianus was closely related to B. exustus I, a species with which it exhibits an antitropical distribution. Their divergence time was approximately 2.6 Ma, consistent with the intensification of Amazon River flow. Brachidontes darwinianus, an estuarine species is shown here not to be related to this B. exustus complex. We suspect ancestral forms may have dispersed from the Caribbean to the Atlantic coast via the Trans-Amazonian seaway (Miocene). The third species, B rodriguezii is presumed to have a long history in the region with related fossil forms going back to the Miocene. Although scorched mussels are very similar in appearance, their evolutionary histories are very different, involving major historical contingencies as the formation of the Amazon River, the Panama Isthmus, and the last marine transgression.
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http://dx.doi.org/10.1002/ece3.2016DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4758806PMC
March 2016

Effective number of breeders, effective population size and their relationship with census size in an iteroparous species, Salvelinus fontinalis.

Proc Biol Sci 2016 01;283(1823)

Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada B3H4R2.

The relationship between the effective number of breeders (Nb) and the generational effective size (Ne) has rarely been examined empirically in species with overlapping generations and iteroparity. Based on a suite of 11 microsatellite markers, we examine the relationship between Nb, Ne and census population size (Nc) in 14 brook trout (Salvelinus fontinalis) populations inhabiting 12 small streams in Nova Scotia and sampled at least twice between 2009 and 2015. Unbiased estimates of Nb obtained with individuals of a single cohort, adjusted on the basis of age at first maturation (α) and adult lifespan (AL), were from 1.66 to 0.24 times the average estimates of Ne obtained with random samples of individuals of mixed ages (i.e. [Formula: see text]). In turn, these differences led to adjusted Ne estimates that were from nearly five to 0.7 times the estimates derived from mixed-aged individuals. These differences translate into the same range of variation in the ratio of effective to census population size [Formula: see text] within populations. Adopting [Formula: see text] as the more precise and unbiased estimates, we found that these brook trout populations differ markedly in their effective to census population sizes (range approx. 0.3 to approx. 0.01). Using AgeNe, we then showed that the variance in reproductive success or reproductive skew varied among populations by a factor of 40, from Vk/k ≈ 5 to 200. These results suggest wide differences in population dynamics, probably resulting from differences in productivity affecting the intensity of competition for access to mates or redds, and thus reproductive skew. Understanding the relationship between Ne, Nb and Nc, and how these relate to population dynamics and fluctuations in population size, are important for the design of robust conservation strategies in small populations with overlapping generations and iteroparity.
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http://dx.doi.org/10.1098/rspb.2015.2601DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4795031PMC
January 2016

The complete mitochondrial genome of the freshwater fish Galaxias platei and a comparison with other species of the genus Galaxias (faraway, so close?).

Mitochondrial DNA A DNA Mapp Seq Anal 2017 03 21;28(2):176-177. Epub 2015 Dec 21.

a Department of Biology , Dalhousie University , Halifax , Nova Scotia , Canada.

We present the whole mitochondrial genome for Galaxias platei, a freshwater fish widely distributed throughout the Patagonian Andes, and compare it with the mitochondrial genome of three congeneric species. The position of G. platei in the phylogenetic reconstruction differs from that shown by earlier studies using multiple markers. We discuss the results in terms of the phylogenetic position of G. platei and the use of whole mitochondrial genomes versus specific regions of multiple organelles.
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http://dx.doi.org/10.3109/19401736.2015.1115497DOI Listing
March 2017

Echoes of a distant time: effects of historical processes on contemporary genetic patterns in Galaxias platei in Patagonia.

Mol Ecol 2015 Aug 30;24(16):4112-28. Epub 2015 Jul 30.

Department of Biology, Dalhousie University, 1355 Oxford St., Halifax, NS, Canada.

Interpreting the genetic structure of a metapopulation as the outcome of gene flow over a variety of timescales is essential for the proper understanding of how changes in landscape affect biological connectivity. Here we contrast historical and contemporary connectivity in two metapopulations of the freshwater fish Galaxias platei in northern and southernmost Patagonia where paleolakes existed during the Holocene and Pleistocene, respectively. Contemporary gene flow was mostly high and asymmetrical in the northern system while extremely reduced in the southernmost system. Historical migration patterns were high and symmetric in the northern system and high and largely asymmetric in the southern system. Both systems showed a moderate structure with a clear pattern of isolation by distance (IBD). Effective population sizes were smaller in populations with low contemporary gene flow. An approximate Bayesian computation (ABC) approach suggests a late Holocene colonization of the lakes in the northern system and recent divergence of the populations from refugial populations from east and west of the Andes. For the southern system, the ABC approach reveals that some of the extant G. platei populations most likely derive from an ancestral population inhabiting a large Pleistocene paleolake while the rest derive from a higher-altitude lake. Our results suggest that neither historical nor contemporary processes individually fully explain the observed structure and geneflow patterns and both are necessary for a proper understanding of the factors that affect diversity and its distribution. Our study highlights the importance of a temporal perspective on connectivity to analyse the diversity of spatially complex metapopulations.
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http://dx.doi.org/10.1111/mec.13303DOI Listing
August 2015

Scorched mussels (BIVALVIA: MYTILIDAE: BRACHIDONTINAE) from the temperate coasts of South America: phylogenetic relationships, trans-Pacific connections and the footprints of Quaternary glaciations.

Mol Phylogenet Evol 2015 Jan 14;82 Pt A:60-74. Epub 2014 Oct 14.

Centro Nacional Patagónico (CONICET), Boulevard Brown 2915, U9120ACF Puerto Madryn, Chubut, Argentina. Electronic address:

This study addresses aspects of the phylogeny and phylogeography of scorched mussels (BIVALVIA: MYTILIDAE: BRACHIDONTINAE) from southern South America (Argentina and Chile), as well as their ecophylogenetic implications. Relationships were inferred from sequences of two nuclear (28S and 18S) and one mitochondrial (COI) genes, using Bayesian and maximum likelihood analyses. Our results indicate that the monophyletic BRACHIDONTINAE include three well supported clades: [i] Brachidontes Swainson (=Hormomya Mörch), [ii] Ischadium Jukes-Browne+Geukensia van de Poel, and [iii] Austromytilus Laseron+Mytilisepta Habe (usually considered a member of the SEPTIFERINAE)+Perumytilus Olsson. Species of clade [iii] are distributed along the temperate coasts of the Pacific Ocean. Available evidence supports divergence between Austromytilus (Australia) and Perumytilus (South American) following the breakup of Australian, Antarctic and South American shelves. Four brachidontins occur in southern South America: Brachidontes rodriguezii (d'Orbigny), B. granulatus (Hanley), and two genetically distinct clades of Perumytilus. The latter are confined to the Chile-Peru (North Clade) and Magellanic (South Clade) Biogeographic Provinces, respectively warm- and cold-temperate. The South Clade is the only brachidontin restricted to cold-temperate waters. Biogeographic considerations and the fossil record prompted the hypothesis that the South Clade originated from the North Clade by incipient peripatric differentiation, followed by isolation during the Quaternary glaciations, genetic differentiation in the non-glaciated coasts of eastern Patagonia, back-expansion over southern Chile following post-LGM de-glaciation, and development of a secondary contact zone between the two clades in south-central Chile. Evidence of upper Pleistocene expansion of the South Clade parallels similar results on other organisms that have colonized coastal ecosystems from eastern Patagonia since the LGM, apparently occupying free ecological space. We emphasize that the assembly of communities cannot be explained solely in terms of environmental drivers, as history also matters.
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http://dx.doi.org/10.1016/j.ympev.2014.10.002DOI Listing
January 2015

Long distance linkage disequilibrium and limited hybridization suggest cryptic speciation in atlantic cod.

PLoS One 2014 26;9(9):e106380. Epub 2014 Sep 26.

Marine Gene Probe Laboratory, Department of Biology, Dalhousie University, Halifax, Nova Scotia.

Hybrid zones provide unprecedented opportunity for the study of the evolution of reproductive isolation, and the extent of hybridization across individuals and genomes can illuminate the degree of isolation. We examine patterns of interchromosomal linkage disequilibrium (ILD) and the presence of hybridization in Atlantic cod, Gadus morhua, in previously identified hybrid zones in the North Atlantic. Here, previously identified clinal loci were mapped to the cod genome with most (∼70%) occurring in or associated with (<5 kb) coding regions representing a diverse array of possible functions and pathways. Despite the observation that clinal loci were distributed across three linkage groups, elevated ILD was observed among all groups of clinal loci and strongest in comparisons involving a region of low recombination along linkage group 7. Evidence of ILD supports a hypothesis of divergence hitchhiking transitioning to genome hitchhiking consistent with reproductive isolation. This hypothesis is supported by Bayesian characterization of hybrid classes present and we find evidence of common F1 hybrids in several regions consistent with frequent interbreeding, yet little evidence of F2 or backcrossed individuals. This work suggests that significant barriers to hybridization and introgression exist among these co-occurring groups of cod either through strong selection against hybrid individuals, or genetic incompatibility and intrinsic barriers to hybridization. In either case, the presence of strong clinal trends, and little gene flow despite extensive hybridization supports a hypothesis of reproductive isolation and cryptic speciation in Atlantic cod. Further work is required to test the degree and nature of reproductive isolation in this species.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0106380PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4178228PMC
June 2015

Genomic islands of divergence and their consequences for the resolution of spatial structure in an exploited marine fish.

Evol Appl 2013 Apr 21;6(3):450-61. Epub 2013 Jan 21.

Fisheries and Oceans Canada St. John's, NF, Canada ; Department of Biology, Marine Gene Probe Laboratory, Dalhousie University Halifax, NS, Canada ; Ocean Sciences Center and Biology Department, Memorial University of Newfoundland St. John's, NF, Canada.

As populations diverge, genomic regions associated with adaptation display elevated differentiation. These genomic islands of adaptive divergence can inform conservation efforts in exploited species, by refining the delineation of management units, and providing genomic tools for more precise and effective population monitoring and the successful assignment of individuals and products. We explored heterogeneity in genomic divergence and its impact on the resolution of spatial population structure in exploited populations of Atlantic cod, Gadus morhua, using genome wide expressed sequence derived single nucleotide polymorphisms in 466 individuals sampled across the range. Outlier tests identified elevated divergence at 5.2% of SNPs, consistent with directional selection in one-third of linkage groups. Genomic regions of elevated divergence ranged in size from a single position to several cM. Structuring at neutral loci was associated with geographic features, whereas outlier SNPs revealed genetic discontinuities in both the eastern and western Atlantic. This fine-scale geographic differentiation enhanced assignment to region of origin, and through the identification of adaptive diversity, fundamentally changes how these populations should be conserved. This work demonstrates the utility of genome scans for adaptive divergence in the delineation of stock structure, the traceability of individuals and products, and ultimately a role for population genomics in fisheries conservation.
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http://dx.doi.org/10.1111/eva.12026DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3673473PMC
April 2013

Contemporary effective population and metapopulation size (N e and meta-N e): comparison among three salmonids inhabiting a fragmented system and differing in gene flow and its asymmetries.

Ecol Evol 2013 Mar 1;3(3):569-80. Epub 2013 Feb 1.

Department of Biology, Dalhousie University Halifax, NS, Canada, B3H 4R2.

We estimated local and metapopulation effective sizes ([Formula: see text] and meta-[Formula: see text]) for three coexisting salmonid species (Salmo salar, Salvelinus fontinalis, Salvelinus alpinus) inhabiting a freshwater system comprising seven interconnected lakes. First, we hypothesized that [Formula: see text] might be inversely related to within-species population divergence as reported in an earlier study (i.e., FST: S. salar> S. fontinalis> S. alpinus). Using the approximate Bayesian computation method implemented in ONeSAMP, we found significant differences in [Formula: see text] ([Formula: see text]) between species, consistent with a hierarchy of adult population sizes ([Formula: see text]). Using another method based on a measure of linkage disequilibrium (LDNE: [Formula: see text]), we found more finite [Formula: see text] values for S. salar than for the other two salmonids, in line with the results above that indicate that S. salar exhibits the lowest [Formula: see text] among the three species. Considering subpopulations as open to migration (i.e., removing putative immigrants) led to only marginal and non-significant changes in [Formula: see text], suggesting that migration may be at equilibrium between genetically similar sources. Second, we hypothesized that meta-[Formula: see text] might be significantly smaller than the sum of local [Formula: see text]s (null model) if gene flow is asymmetric, varies among subpopulations, and is driven by common landscape features such as waterfalls. One 'bottom-up' or numerical approach that explicitly incorporates variable and asymmetric migration rates showed this very pattern, while a number of analytical models provided meta-[Formula: see text] estimates that were not significantly different from the null model or from each other. Our study of three species inhabiting a shared environment highlights the importance and utility of differentiating species-specific and landscape effects, not only on dispersal but also in the demography of wild populations as assessed through local [Formula: see text]s and meta-[Formula: see text]s and their relevance in ecology, evolution and conservation.
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http://dx.doi.org/10.1002/ece3.485DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3605847PMC
March 2013

Mature male parr contribution to the effective size of an anadromous Atlantic salmon (Salmo salar) population over 30 years.

Mol Ecol 2013 May 14;22(9):2394-407. Epub 2013 Jan 14.

Department of Biology, Dalhousie University, Halifax, NS, Canada.

We describe temporal changes in the genetic composition of a small anadromous Atlantic salmon (Salmo salar) population from South Newfoundland, an area where salmon populations are considered threatened (COSEWIC 2010). We examined the genetic variability (13 microsatellite loci) in 869 out-migrating smolt and post-spawning kelt samples, collected from 1985 to 2011 for a total of 22 annual collections and a 30 year span of assigned cohorts. We estimated the annual effective number of breeders (Nb) and the generational effective population size (Ne) through genetic methods and demographically using the adult sex ratio. Comparisons between genetic and demographic estimates show that the adult spawners inadequately explain the observed Ne estimates, suggesting that mature male parr are significantly increasing Nb and Ne over the study period. Spawning as parr appears to be a viable and important strategy in the near absence of adult males.
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http://dx.doi.org/10.1111/mec.12186DOI Listing
May 2013

Poleward bound: biological impacts of Southern Hemisphere glaciation.

Trends Ecol Evol 2012 Aug 31;27(8):462-71. Epub 2012 May 31.

Lutte Biologique et Ecologie Spatiale, Université Libre de Bruxelles, 50 av FD Roosevelt - CP 160/12, 1050 Bruxelles, Belgium.

Postglacial recolonisation patterns are well documented for the Northern Hemisphere biota, but comparable processes in the Southern Hemisphere have only recently been examined. In the largely terrestrial Northern Hemisphere, recession of ice after the Last Glacial Maximum (LGM) allowed various taxa, including slow-moving terrestrial species, to migrate poleward. By contrast, the Southern Hemisphere polar region is completely ringed by ocean, and recolonisation of Antarctica and the sub-Antarctic islands has thus presented considerable challenges. Although a few highly dispersive marine species have been able to recolonise postglacially, most surviving high-latitude taxa appear to have persisted throughout glacial maxima in local refugia. These contrasting patterns highlight the importance of habitat continuity in facilitating biological range shifts in response to climate change.
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http://dx.doi.org/10.1016/j.tree.2012.04.011DOI Listing
August 2012

Permanent genetic resources added to Molecular Ecology Resources Database 1 December 2011-31 January 2012.

Mol Ecol Resour 2012 May 26;12(3):570-2. Epub 2012 Mar 26.

This article documents the addition of 473 microsatellite marker loci and 71 pairs of single-nucleotide polymorphism (SNP) sequencing primers to the Molecular Ecology Resources Database. Loci were developed for the following species: Barteria fistulosa, Bombus morio, Galaxias platei, Hematodinium perezi, Macrocentrus cingulum Brischke (a.k.a. M. abdominalis Fab., M. grandii Goidanich or M. gifuensis Ashmead), Micropogonias furnieri, Nerita melanotragus, Nilaparvata lugens Stål, Sciaenops ocellatus, Scomber scombrus, Spodoptera frugiperda and Turdus lherminieri. These loci were cross-tested on the following species: Barteria dewevrei, Barteria nigritana, Barteria solida, Cynoscion acoupa, Cynoscion jamaicensis, Cynoscion leiarchus, Cynoscion nebulosus, Cynoscion striatus, Cynoscion virescens, Macrodon ancylodon, Menticirrhus americanus, Nilaparvata muiri and Umbrina canosai. This article also documents the addition of 116 sequencing primer pairs for Dicentrarchus labrax.
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http://dx.doi.org/10.1111/j.1755-0998.2012.03133.xDOI Listing
May 2012

Climate-induced changes to the ancestral population size of two Patagonian galaxiids: the influence of glacial cycling.

Mol Ecol 2011 Dec 11;20(24):5280-94. Epub 2011 Nov 11.

Department of Biology, Dalhousie University, Halifax, NS, Canada.

Patagonia is one of the few areas in the Southern Hemisphere to have been directly influenced by Quaternary glaciers. In this study, we evaluate the influence that Quaternary glacial ice had on the genetic diversity of two congeneric fish species, the diadromous Galaxias maculatus and the nondiadromous Galaxias platei, using multilocus estimates of effective population size through time. Mid-Quaternary glaciations had far-reaching consequences for both species. Galaxias maculatus and G. platei each experienced severe genetic bottlenecks during the period when Patagonia ice sheet advance reached its maximum positions c. 1.1-0.6 Ma. Concordant drops in effective size during this time suggest that range sizes were under similar constraints. It is therefore unlikely that coastal (brackish/marine) environments served as a significant refuge for G. maculatus during glacial periods. An earlier onset of population declines for G. platei suggests that this species was vulnerable to modest glacial advances. Declines in effective sizes were continuous for both species and lasted into the late-Pleistocene. However, G. maculatus exhibited a strong population recovery during the late-Quaternary (c. 400,000 bp). Unusually long and warm interglacials associated with the late-Quaternary may have helped to facilitate a strong population rebound in this primarily coastal species.
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http://dx.doi.org/10.1111/j.1365-294X.2011.05352.xDOI Listing
December 2011

Historical changes in genotypic frequencies at the Pantophysin locus in Atlantic cod (Gadus morhua) in Icelandic waters: evidence of fisheries-induced selection?

Evol Appl 2011 Jul 5;4(4):562-73. Epub 2011 Jan 5.

Institute of Biology, University of Iceland Reykjavik, Iceland.

The intense fishing mortality imposed on Atlantic cod in Icelandic waters during recent decades has resulted in marked changes in stock abundance, as well as in age and size composition. Using a molecular marker known to be under selection (Pan I) along with a suite of six neutral microsatellite loci, we analysed an archived data set and revealed evidence of distinct temporal changes in the frequencies of genotypes at the Pan I locus among spawning Icelandic cod, collected between 1948 and 2002, a period characterized by high fishing pressure. Concurrently, temporal stability in the composition of the microsatellite loci was established within the same data set. The frequency of the Pan I(BB) genotype decreased over a period of six decades, concomitant with considerable spatial and technical changes in fishing effort that resulted in the disappearance of older individuals from the fishable stock. Consequently, these changes have likely led to a change in the genotype frequencies at this locus in the spawning stock of Icelandic cod. The study highlights the value of molecular genetic approaches that combine functional and neutral markers examined in the same set of individuals for investigations of the selective effects of harvesting and reiterates the need for an evolutionary dimension to fisheries management.
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http://dx.doi.org/10.1111/j.1752-4571.2010.00176.xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3352422PMC
July 2011

Understanding and estimating effective population size for practical application in marine species management.

Conserv Biol 2011 Jun 1;25(3):438-49. Epub 2011 Feb 1.

Department of Natural Resources, Cornell University, Ithaca NY 14853, USA.

Effective population size (N(e)) determines the strength of genetic drift in a population and has long been recognized as an important parameter for evaluating conservation status and threats to genetic health of populations. Specifically, an estimate of N(e) is crucial to management because it integrates genetic effects with the life history of the species, allowing for predictions of a population's current and future viability. Nevertheless, compared with ecological and demographic parameters, N(e) has had limited influence on species management, beyond its application in very small populations. Recent developments have substantially improved N(e) estimation; however, some obstacles remain for the practical application of N(e) estimates. For example, the need to define the spatial and temporal scale of measurement makes the concept complex and sometimes difficult to interpret. We reviewed approaches to estimation of N(e) over both long-term and contemporary time frames, clarifying their interpretations with respect to local populations and the global metapopulation. We describe multiple experimental factors affecting robustness of contemporary N(e) estimates and suggest that different sampling designs can be combined to compare largely independent measures of N(e) for improved confidence in the result. Large populations with moderate gene flow pose the greatest challenges to robust estimation of contemporary N(e) and require careful consideration of sampling and analysis to minimize estimator bias. We emphasize the practical utility of estimating N(e) by highlighting its relevance to the adaptive potential of a population and describing applications in management of marine populations, where the focus is not always on critically endangered populations. Two cases discussed include the mechanisms generating N(e) estimates many orders of magnitude lower than census N in harvested marine fishes and the predicted reduction in N(e) from hatchery-based population supplementation.
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http://dx.doi.org/10.1111/j.1523-1739.2010.01637.xDOI Listing
June 2011