Michael E. Pfrender

The ecoresponsive genome of Daphnia pulex

The Daphnia genome reveals a multitude of genes and shows adaptation through gene family expansions. We describe the draft genome of the microcrustacean Daphnia pulex, which is only 200 megabases and contains at least 30,907 genes. The high gene count is a consequence of an elevated rate of gene duplication resulting in tandem gene clusters. More than a third of Daphnia’s genes have no detectable homologs in any other available proteome, and the most amplified gene families are specific to the Daphnia lineage. The coexpansion of gene families interacting within metabolic pathways suggests that the maintenance of duplicated genes is not random, and the analysis of gene expression under different environmental conditions reveals that numerous paralogs acquire divergent expression patterns soon after duplication. Daphnia-specific genes, including many additional loci within sequenced regions that are otherwise devoid of annotations, are the most responsive genes to ecological challenges.

The adaptive landscape as a conceptual bridge between micro- and macroevolution

An adaptive landscape concept outlined by G.G. Simpson constitutes the major conceptual bridge between the fields of micro- and macroevolutionary study. Despite some important theoretical extensions since 1944, this conceptual bridge has been ignored in many empirical studies. In this article, we review the status of theoretical work and emphasize the importance of models for peak movement. Although much theoretical work has been devoted to evolution on stationary, unchanging landscapes, an important new development is a focus on the evolution of the landscape itself. We also sketch an agenda of empirical issues that is inspired by theoretical developments.

THE QUANTITATIVE AND MOLECULAR GENETIC ARCHITECTURE OF A SUBDIVIDED SPECIES

In an effort to elucidate the evolutionary mechanisms that determine the genetic architecture of a species, we have analyzed 17 populations of the microcrustacean Daphnia pulex for levels of genetic variation at the level of life‐history characters and molecular markers in the nuclear and mitochondrial genomes. This species is highly subdivided, with approximately 30% of the variation for nuclear molecular markers and 50% of the variation for mitochondrial markers being distributed among populations. The average level of genetic subdivision for quantitative traits is essentially the same as that for nuclear markers, which superficially suggests that the life‐history characters are diverging at the neutral rate. However, the existence of a strong correlation between the levels of population subdivision and broadsense heritabilities of individual traits argues against this interpretation, suggesting instead that the among‐population divergence of some quantitative traits (most notably body size) is being driven by local adaptation to different environments. The fact that the mean phenotypes of the individual populations are also strongly correlated with local levels of homozygosity indicates that variation in local inbreeding plays a role in population differentiation. Rather than being a passive consequence of local founder effects, levels of homozygosity may be selected for directly for their effects on the phenotype (adaptive inbreeding depression). There is no relationship between the levels of variation within populations for molecular markers and quantitative characters, and this is explained by the fact that the average standing genetic variation for life‐history characters in this species is equivalent to only 33 generations of variation generated by mutation.

The i5K Initiative: Advancing Arthropod Genomics for Knowledge, Human Health, Agriculture, and the Environment

Insects and their arthropod relatives including mites, spiders, and crustaceans play major roles in the worlds terrestrial, aquatic, and marine ecosystems. Arthropods compete with humans for food and transmit devastating diseases. They also comprise the most diverse and successful branch of metazoan evolution, with millions of extant species. Here, we describe an international effort to guide arthropod genomic efforts, from species prioritization to methodology and informatics. The 5000 arthropod genomes initiative (i5K) community met formally in 2012 to discuss a roadmap for sequencing and analyzing 5000 high-priority arthropods and is continuing this effort via pilot projects, the development of standard operating procedures, and training of students and career scientists. With university, governmental, and industry support, the i5K Consortium aspires to deliver sequences and analytical tools for each of the arthropod branches and each of the species having beneficial and negative effects on humankind.

Conservation in a cup of water: estimating biodiversity and population abundance from environmental DNA

Three mantras often guide species and ecosystem management: (i) for preventing invasions by harmful species, ‘early detection and rapid response’; (ii) for conserving imperilled native species, ‘protection of biodiversity hotspots’; and (iii) for assessing biosecurity risk, ‘an ounce of prevention equals a pound of cure.’ However, these and other management goals are elusive when traditional sampling tools (e.g. netting, traps, electrofishing, visual surveys) have poor detection limits, are too slow or are not feasible. One visionary solution is to use an organism’s DNA in the environment (eDNA), rather than the organism itself, as the target of detection. In this issue of Molecular Ecology, Thomsen et al. (2012) provide new evidence demonstrating the feasibility of this approach, showing that eDNA is an accurate indicator of the presence of an impressively diverse set of six aquatic or amphibious taxa including invertebrates, amphibians, a fish and a mammal in a wide range of freshwater habitats. They are also the first to demonstrate that the abundance of eDNA, as measured by qPCR, correlates positively with population abundance estimated with traditional tools. Finally, Thomsen et al. (2012) demonstrate that next‐generation sequencing of eDNA can quantify species richness. Overall, Thomsen et al. (2012) provide a revolutionary roadmap for using eDNA for detection of species, estimates of relative abundance and quantification of biodiversity.

Phenotypic plasticity facilitates recurrent rapid adaptation to introduced predators

A central role for phenotypic plasticity in adaptive evolution is often posited yet lacks empirical support. Selection for the stable production of an induced phenotype is hypothesized to modify the regulation of preexisting developmental pathways, producing rapid adaptive change. We examined the role of plasticity in rapid adaptation of the zooplankton Daphnia melanica to novel fish predators. Here we show that plastic up-regulation of the arthropod melanin gene dopa decarboxylase (Ddc) in the absence of UV radiation is associated with reduced pigmentation in D. melanica. Daphnia populations coexisting with recently introduced fish exhibit environmentally invariant up-regulation of Ddc, accompanied by constitutive up-regulation of the interacting arthropod melanin gene ebony. Both changes in regulation are associated with adaptive reduction in the plasticity and mean expression of melanin. Our results provide evidence that the developmental mechanism underlying ancestral plasticity in response to an environmental factor has been repeatedly co-opted to facilitate rapid adaptation to an introduced predator.

Mitochondrial DNA variation, phylogeography and population structure of the Asian elephant

We report the first genetic analysis of free-ranging Asian elephants (Elephas maximus). We sampled 118 elephants from Sri Lanka, Bhutan/North India, and Laos/Vietnam by extracting DNA from dung, PCR amplifying and sequencing 630 nucleotides of mitochondrial DNA, including part of the variable left domain of the control region. Comparison with African elephant (Loxodonta africana) sequences indicated a relatively slow molecular clock in the Proboscidea with a sequence divergence of ≈1%/Myr. Genetic diversity within Asian elephants was low, suggesting a small long-term effective population size. Seventeen haplotypes were identified within Asian elephants, which clustered into two well-differentiated assemblages with an estimated Pliocene divergence of 2.5–3.5 million years ago. The two assemblages showed incomplete geographical partitioning, suggesting allopatric divergence and secondary admixture. On the mainland, little genetic differentiation was observed between elephant populations of Bhutan and India or Laos and Vietnam. A significant difference in haplotype frequencies but relatively weak subdivision was observed between the regions Bhutan–India and Laos–Vietnam. Significant genetic differentiation was observed between the mainland and Sri Lanka, and between northern, mid-latitude and southern regions in Sri Lanka.

Linking genes to communities and ecosystems: Daphnia as an ecogenomic model

How do genetic variation and evolutionary change in critical species affect the composition and functioning of populations, communities and ecosystems? Illuminating the links in the causal chain from genes up to ecosystems is a particularly exciting prospect now that the feedbacks between ecological and evolutionary changes are known to be bidirectional. Yet to fully explore phenomena that span multiple levels of the biological hierarchy requires model organisms and systems that feature a comprehensive triad of strong ecological interactions in nature, experimental tractability in diverse contexts and accessibility to modern genomic tools. The water flea Daphnia satisfies these criteria, and genomic approaches capitalizing on the pivotal role Daphnia plays in the functioning of pelagic freshwater food webs will enable investigations of eco-evolutionary dynamics in unprecedented detail. Because its ecology is profoundly influenced by both genetic polymorphism and phenotypic plasticity, Daphnia represents a model system with tremendous potential for developing a mechanistic understanding of the relationship between traits at the genetic, organismal and population levels, and consequences for community and ecosystem dynamics. Here, we highlight the combination of traits and ecological interactions that make Daphnia a definitive model system, focusing on the additional power and capabilities enabled by recent molecular and genomic advances.

Quantification of mesocosm fish and amphibian species diversity via environmental DNA metabarcoding.

Freshwater fauna are particularly sensitive to environmental change and disturbance. Management agencies frequently use fish and amphibian biodiversity as indicators of ecosystem health and a way to prioritize and assess management strategies. Traditional aquatic bioassessment that relies on capture of organisms via nets, traps and electrofishing gear typically has low detection probabilities for rare species and can injure individuals of protected species. Our objective was to determine whether environmental DNA (eDNA) sampling and metabarcoding analysis can be used to accurately measure species diversity in aquatic assemblages with differing structures. We manipulated the density and relative abundance of eight fish and one amphibian species in replicated 206‐L mesocosms. Environmental DNA was filtered from water samples, and six mitochondrial gene fragments were Illumina‐sequenced to measure species diversity in each mesocosm. Metabarcoding detected all nine species in all treatment replicates. Additionally, we found a modest, but positive relationship between species abundance and sequencing read abundance. Our results illustrate the potential for eDNA sampling and metabarcoding approaches to improve quantification of aquatic species diversity in natural environments and point the way towards using eDNA metabarcoding as an index of macrofaunal species abundance.

The evolutionary origins of beneficial alleles during the repeated adaptation of garter snakes to deadly prey

Where do the genetic variants underlying adaptive change come from? Are currently adaptive alleles recruited by selection from standing genetic variation within populations, moved through introgression from other populations, or do they arise as novel mutations? Here, we examine the molecular basis of repeated adaptation to the toxin of deadly prey in 3 species of garter snakes (Thamnophis) to determine whether adaptation has evolved through novel mutations, sieving of existing variation, or transmission of beneficial alleles across species. Functional amino acid substitutions in the skeletal muscle sodium channel (Nav1.4) are largely responsible for the physiological resistance of garter snakes to tetrodotoxin found in their newt (Taricha) prey. Phylogenetic analyses reject the hypotheses that the unique resistance alleles observed in multiple Thamnophis species were present before the split of these lineages, or that alleles were shared among species through occasional hybridization events. Our results demonstrate that adaptive evolution has occurred independently multiple times in garter snakes via the de novo acquisition of beneficial mutations.