Jennifer A. Jackson

Neglect of Genetic Diversity in Implementation of the Convention on Biological Diversity

Genetic diversity is the foundation for all biological diversity; the persistence and evolutionary potential of species depend on it. World leaders have agreed on the conservation of genetic diversity as an explicit goal of the Convention on Biological Diversity (CBD). Nevertheless, actions to protect genetic diversity are largely lacking. With only months left to the 2010-biodiversity target, when the 191 parties to the CBD have agreed on achieving a significant reduction of the rate of biodiversity loss, gene-level diversity is still not being monitored, and indicators and thresholds that can be used to devise strategies to conserve this important component of biodiversity are missing. Immediate action is needed to ensure that genetic diversity is not neglected in conservation targets beyond 2010.

When are genetic methods useful for estimating contemporary abundance and detecting population trends

The utility of microsatellite markers for inferring population size and trend has not been rigorously examined, even though these markers are commonly used to monitor the demography of natural populations. We assessed the ability of a linkage disequilibrium estimator of effective population size (Ne) and a simple capture‐recapture estimator of abundance (N) to quantify the size and trend of stable or declining populations (true Nu2003=u2003100–10,000), using simulated Wright–Fisher populations. Neither method accurately or precisely estimated abundance at sample sizes of Su2003=u200330 individuals, regardless of true N. However, if larger samples of Su2003=u200360 or 120 individuals were collected, these methods provided useful insights into abundance and trends for populations of Nu2003=u2003100–500. At small population sizes (Nu2003=u2003100 or 250), precision of the Ne estimates was improved slightly more by a doubling of loci sampled than by a doubling of individuals sampled. In general, monitoring Ne proved a more robust means of identifying stable and declining populations than monitoring N over most of the parameter space we explored, and performance of the Ne estimator is further enhanced if the Ne/N ratio is low. However, at the largest population size (Nu2003=u200310,000), N estimation outperformed Ne. Both methods generally required ≥u20035 generations to pass between sampling events to correctly identify population trend.

Applied Conservation Genetics and the Need for Quality Control and Reporting of Genetic Data Used in Fisheries and Wildlife Management

Genetic data are often critical for defining populations for management purposes (e.g., identifying geographic boundaries or diagnostic characters for genetically discrete subunits) but can be called into question by both scientific and legal review. This can result in reversed or delayed implementation of management actions. We discuss methods for data quality control and quality analysis and describe examples of steps applied to 2 of the most common types of genetic data, mitochondrial DNA sequences, and microsatellite genotypes. These steps can serve both as guides to conservation geneticists and as an initial protocol for managers to determine whether genetic data will hold up against legal and scientific challenges. In addition, we suggest types of data and quality measures that should be reported as supplementary materials to published reports. These supplementary data serve to reduce the occurrence of legal and conservation controversies and improve reproducibility over time in population genetics studies where genetic monitoring is likely to play an increasing role.

Big and Slow: Phylogenetic estimates of molecular evolution in baleen whales (Suborder Mysticeti)

Baleen whales are the largest animals that have ever lived. To develop an improved estimation of substitution rate for nuclear and mitochondrial DNA for this taxon, we implemented a relaxed-clock phylogenetic approach using three fossil calibration dates: the divergence between odontocetes and mysticetes approximately 34 million years ago (Ma), between the balaenids and balaenopterids approximately 28 Ma, and the time to most recent common ancestor within the Balaenopteridae approximately 12 Ma. We examined seven mitochondrial genomes, a large number of mitochondrial control region sequences (219 haplotypes for 465 bp) and nine nuclear introns representing five species of whales, within which multiple species-specific alleles were sequenced to account for within-species diversity (1-15 for each locus). The total data set represents >1.65 Mbp of mitogenome and nuclear genomic sequence. The estimated substitution rate for the humpback whale control region (3.9%/million years, My) was higher than previous estimates for baleen whales but slow relative to other mammal species with similar generation times (e.g., human-chimp mean rate > 20%/My). The mitogenomic third codon position rate was also slow relative to other mammals (mean estimate 1%/My compared with a mammalian average of 9.8%/My for the cytochrome b gene). The mean nuclear genomic substitution rate (0.05%/My) was substantially slower than average synonymous estimates for other mammals (0.21-0.37%/My across a range of studies). The nuclear and mitogenome rate estimates for baleen whales were thus roughly consistent with an 8- to 10-fold slowing due to a combination of large body size and long generation times. Surprisingly, despite the large data set of nuclear intron sequences, there was only weak and conflicting support for alternate hypotheses about the phylogeny of balaenopterid whales, suggesting that interspecies introgressions or a rapid radiation has obscured species relationships in the nuclear genome.

Divergence time estimates for major cephalopod groups: evidence from multiple genes

This is the first study to use both molecular and fossil data to date the divergence of taxa within the coleoid cephalopods (octopus, squid, cuttlefish). A dataset including sequences from three nuclear and three mitochondrial genes (3415u2003bp in total) was used to investigate the evolutionary divergences within the group. Divergence time analyses were performed using the Thorne/Kishino method of analysis which allows multiple constraints from the fossil record and permits rates of molecular evolution to vary on different branches of a phylogenetic tree. The data support a Paleozoic origin of the Orders Vampyromorpha, Octopoda and the majority of the extant higher level decapodiform taxa. These estimated divergence times are considerably older than paleontological estimates. The major lineages within the Order Octopoda were estimated to have diverged in the Mesozoic, with a radiation of many taxa around the Cretaceous/Cenozoic boundary. Higher level decapodiform phylogenetic relationships appear to have been obscured due to an ancient diversification of this group.

How few whales were there after whaling? Inference from contemporary mtDNA diversity

Reconstructing the history of exploited populations of whales requires fitting a trajectory through at least three points in time: (i) prior to exploitation, when abundance is assumed to be at the maximum allowed by environmental carrying capacity; (ii) the point of minimum abundance or ‘bottleneck’, usually near the time of protection or the abandonment of the hunt; and (iii) near the present, when protected populations are assumed to have undergone some recovery. As historical abundance is usually unknown, this trajectory must be extrapolated according to a population dynamic model using catch records, an assumed rate of increase and an estimate of current abundance, all of which have received considerable attention by the International Whaling Commission (IWC). Relatively little attention has been given to estimating minimum abundance (Nmin), although it is clear that genetic and demographic forces at this point are critical to the potential for recovery or extinction of a local population. We present a general analytical framework to improve estimates of Nmin using the number of mtDNA haplotypes (maternal lineages) surviving in a contemporary population of whales or other exploited species. We demonstrate the informative potential of this parameter as an a posteriori constraint on Bayesian logistic population dynamic models based on the IWC Comprehensive Assessment of the intensively exploited southern right whales (Eubalaena australis) and published surveys of mtDNA diversity for this species. Estimated historical trajectories from all demographic scenarios suggested a substantial loss of mtDNA haplotype richness as a result of 19th century commercial whaling and 20th century illegal whaling by the Soviet Union. However, the relatively high rates of population increase used by the IWC assessment predicted a bottleneck that was implausibly narrow (median, 67 mature females), given our corrected estimates of Nmin. Further, high levels of remnant sequence diversity (theta) suggested that pre‐exploitation abundance was larger than predicted by the logistic model given the catch record, which is known to be incomplete. Our results point to a need to better integrate evolutionary processes into population dynamic models to account for uncertainty in catch records, the influence of maternal fidelity on metapopulation dynamics, and the potential for inverse density dependence (an ‘Allee effect’) in severely depleted populations.

Species tree of a recent radiation : the subfamily Delphininae (Cetacea, Mammalia)

Lineages undergoing rapid radiations provide exceptional opportunities for studying speciation and adaptation, but also represent a challenge for molecular systematics because retention of ancestral polymorphisms and the occurrence of hybridization can obscure relationships among lineages. Dolphins in the subfamily Delphininae are one such case. Non-monophyly, rapid speciation events, and discordance between morphological and molecular characters have made the inference of phylogenetic relationships within this subfamily very difficult. Here we approach this problem by applying multiple methods intended to estimate species trees using a multi-gene dataset for the Delphininae (Sousa, Sotalia, Stenella, Tursiops, Delphinus and Lagenodelphis). Incongruent gene trees obtained indicate that incomplete lineage sorting and possibly hybridization are confounding the inference of species history in this group. Nonetheless, using coalescent-based methods, we have been able to extract an underlying species-tree signal from divergent histories of independent genes. This is the first time a molecular study provides support for such relationships. This study further illustrates how methods of species-tree inference can be very sensitive both to the characteristics of the dataset and the evolutionary processes affecting the evolution of the group under study.

Global diversity and oceanic divergence of humpback whales (Megaptera novaeangliae)

Humpback whales (Megaptera novaeangliae) annually undertake the longest migrations between seasonal feeding and breeding grounds of any mammal. Despite this dispersal potential, discontinuous seasonal distributions and migratory patterns suggest that humpbacks form discrete regional populations within each ocean. To better understand the worldwide population history of humpbacks, and the interplay of this species with the oceanic environment through geological time, we assembled mitochondrial DNA control region sequences representing approximately 2700 individuals (465 bp, 219 haplotypes) and eight nuclear intronic sequences representing approximately 70 individuals (3700 bp, 140 alleles) from the North Pacific, North Atlantic and Southern Hemisphere. Bayesian divergence time reconstructions date the origin of humpback mtDNA lineages to the Pleistocene (880 ka, 95% posterior intervals 550–1320 ka) and estimate radiation of current Northern Hemisphere lineages between 50 and 200 ka, indicating colonization of the northern oceans prior to the Last Glacial Maximum. Coalescent analyses reveal restricted gene flow between ocean basins, with long-term migration rates (individual migrants per generation) of less than 3.3 for mtDNA and less than 2 for nuclear genomic DNA. Genetic evidence suggests that humpbacks in the North Pacific, North Atlantic and Southern Hemisphere are on independent evolutionary trajectories, supporting taxonomic revision of M. novaeangliae to three subspecies.

Exploring Pandora's Box: Potential and Pitfalls of Low Coverage Genome Surveys for Evolutionary Biology

High throughput sequencing technologies are revolutionizing genetic research. With this “rise of the machines”, genomic sequences can be obtained even for unknown genomes within a short time and for reasonable costs. This has enabled evolutionary biologists studying genetically unexplored species to identify molecular markers or genomic regions of interest (e.g. micro- and minisatellites, mitochondrial and nuclear genes) by sequencing only a fraction of the genome. However, when using such datasets from non-model species, it is possible that DNA from non-target contaminant species such as bacteria, viruses, fungi, or other eukaryotic organisms may complicate the interpretation of the results. In this study we analysed 14 genomic pyrosequencing libraries of aquatic non-model taxa from four major evolutionary lineages. We quantified the amount of suitable micro- and minisatellites, mitochondrial genomes, known nuclear genes and transposable elements and searched for contamination from various sources using bioinformatic approaches. Our results show that in all sequence libraries with estimated coverage of about 0.02–25%, many appropriate micro- and minisatellites, mitochondrial gene sequences and nuclear genes from different KEGG (Kyoto Encyclopedia of Genes and Genomes) pathways could be identified and characterized. These can serve as markers for phylogenetic and population genetic analyses. A central finding of our study is that several genomic libraries suffered from different biases owing to non-target DNA or mobile elements. In particular, viruses, bacteria or eukaryote endosymbionts contributed significantly (up to 10%) to some of the libraries analysed. If not identified as such, genetic markers developed from high-throughput sequencing data for non-model organisms may bias evolutionary studies or fail completely in experimental tests. In conclusion, our study demonstrates the enormous potential of low-coverage genome survey sequences and suggests bioinformatic analysis workflows. The results also advise a more sophisticated filtering for problematic sequences and non-target genome sequences prior to developing markers.

Are Antarctic minke whales unusually abundant because of 20th century whaling

Severe declines in megafauna worldwide illuminate the role of top predators in ecosystem structure. In the Antarctic, the Krill Surplus Hypothesis posits that the killing of more than 2u2003million large whales led to competitive release for smaller krill‐eating species like the Antarctic minke whale. If true, the current size of the Antarctic minke whale population may be unusually high as an indirect result of whaling. Here, we estimate the long‐term population size of the Antarctic minke whale prior to whaling by sequencing 11 nuclear genetic markers from 52 modern samples purchased in Japanese meat markets. We use coalescent simulations to explore the potential influence of population substructure and find that even though our samples are drawn from a limited geographic area, our estimate reflects ocean‐wide genetic diversity. Using Bayesian estimates of the mutation rate and coalescent‐based analyses of genetic diversity across loci, we calculate the long‐term population size of the Antarctic minke whale to be 670u2003000 individuals (95% confidence interval: 374u2003000–1u2003150u2003000). Our estimate of long‐term abundance is similar to, or greater than, contemporary abundance estimates, suggesting that managing Antarctic ecosystems under the assumption that Antarctic minke whales are unusually abundant is not warranted.