Molecular Ecology (Mol Ecol)

Publications in this journal

• Article: Mass flowering of the tropical tree Shorea beccariana was preceded by expression changes in flowering and drought-responsive genes.

  Masaki J Kobayashi, Yayoi Takeuchi, Tanaka Kenta, Tomonori Kume, Bibian Diway, Kentaro K Shimizu
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  ABSTRACT: Community-level mass flowering, known as general flowering, which occurs in South-East Asia at supra-annual irregular intervals, is considered a particularly spectacular phenomenon in tropical ecology. Recent studies have proposed several proximate factors inducing general flowering, such as drought and falls in minimum temperature. However, limited empirical data on the developmental and physiological processes have been available to test the significance of such factors. To overcome this limitation and test the hypotheses that general flowering is triggered by the proposed factors, we conducted an 'ecological transcriptome' study of a mass flowering species, Shorea beccariana, comparing meteorological data with genome-wide expression patterns obtained using next-generation sequencing. Among the 98 flowering-related genes identified, the homologs of a floral pathway integrator, SbFT, and a floral repressor, SbSVP, showed dramatic transcriptional changes before flowering, and their flowering functions were confirmed using transgenic Arabidopsis thaliana. Expression in drought-responsive and sucrose-induced genes also changed before flowering. All these expression changes occurred when the flowering-inducing level of drought was reached, as estimated using data from the preceding 10 years. These genome-wide expression data support the hypothesis that drought is a trigger for general flowering.
  Molecular Ecology 05/2013;
• Article: Divergence in coloration and ecological speciation in the Anolis marmoratus species complex.

  Martha M Muñoz, Nicholas G Crawford, Thomas J McGreevy, Nicholas J Messana, Rebecca D Tarvin, Liam J Revell, Rosanne M Zandvliet, Juanita M Hopwood, Elbert Mock, André L Schneider, Christopher J Schneider
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  ABSTRACT: Adaptive divergence in coloration is expected to produce reproductive isolation in species that use colourful signals in mate choice and species recognition. Indeed, many adaptive radiations are characterized by differentiation in colourful signals, suggesting that divergent selection acting on coloration may be an important component of speciation. Populations in the Anolis marmoratus species complex from the Caribbean island of Guadeloupe display striking divergence in the colour and pattern of adult males that occurs over small geographic distances, suggesting strong divergent selection. Here we test the hypothesis that divergence in coloration results in reduced gene flow among populations. We quantify variation in adult male coloration across a habitat gradient between mesic and xeric habitats, use a multilocus coalescent approach to infer historical demographic parameters of divergence, and examine gene flow and population structure using microsatellite variation. We find that colour variation evolved without geographic isolation and in the face of gene flow, consistent with strong divergent selection and that both ecological and sexual selection are implicated. However, we find no significant differentiation at microsatellite loci across populations, suggesting little reproductive isolation and high levels of contemporary gene exchange. Strong divergent selection on loci affecting coloration probably maintains clinal phenotypic variation despite high gene flow at neutral loci, supporting the notion of a porous genome in which adaptive portions of the genome remain fixed whereas neutral portions are homogenized by gene flow and recombination. We discuss the impact of these findings for studies of colour evolution and ecological speciation.
  Molecular Ecology 05/2013; 22(10):2668-82.
• Article: Professor godfrey matthew Hewitt (1940-2013).

  Brent Emerson
  Molecular Ecology 05/2013; 22(9):2359-60.
• Article: Nutrient enrichment increased species richness of leaf litter fungal assemblages in a tropical forest.

  Jennifer Kerekes, Michael Kaspari, Bradley Stevenson, R Henrik Nilsson, Martin Hartmann, Anthony Amend, Thomas D Bruns
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  ABSTRACT: Microbial communities play a major role in terrestrial ecosystem functioning, but the determinates of their diversity and functional interactions are not well known. In this study, we explored leaf litter fungal diversity in a diverse Panama lowland tropical forest in which a replicated factorial N, P, K and micronutrient fertilization experiment of 40 × 40 m plots had been ongoing for nine years. We extracted DNA from leaf litter samples and used fungal-specific amplification and a 454 pyrosequencing approach to sequence two loci, the nuclear ribosomal internal transcribed spacer (ITS) region and the nuclear ribosomal large subunit (LSU) D1 region. Using a 95% sequence similarity threshold for ITS1 spacer recovered a total of 2523 OTUs, and the number of unique ITS1 OTUs per 0.5-1.0 g leaf litter sample ranged from 55 to 177. Ascomycota were the dominant phylum among the leaf litter fungi (71% of the OTUs), followed by Basidiomycota (26% of the OTUs). In contrast to our expectations based on temperate ecosystems, long-term addition of nutrients increased, rather than decreased, species richness relative to controls. Effect of individual nutrients was more subtle and seen primarily as changes in community compositions especially at lower taxonomic levels, rather than as significant changes in species richness. For example, plots receiving P tended to show a greater similarity in community composition compared to the other nutrient treatments, the +PK, +NK and +NPK plots appeared to be more dominated by the Nectriaceae than other treatments, and indicator species for particular nutrient combinations were identified.
  Molecular Ecology 04/2013;
• Article: Recombination in the threespine stickleback genome-patterns and consequences.

  Marius Roesti, Dario Moser, Daniel Berner
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  ABSTRACT: Heterogeneity in recombination rate may strongly influence genome evolution and entail methodological challenges to genomic investigation. Nevertheless, a solid understanding of these issues awaits detailed information across a broad range of taxa. Based on 282 F2 individuals and 1872 single nucleotide polymorphisms, we characterize recombination in the threespine stickleback fish genome. We find an average genome-wide recombination rate of 3.11 cm/Mb. Crossover frequencies are dramatically elevated in the chromosome peripheries as compared to the centres, and are consistent with one obligate crossover per chromosome (but not chromosome arm). Along the sex chromosome, we show that recombination is restricted to a small pseudoautosomal domain of c. 2 Mb, spanning only 10% of that chromosome. Comparing female to male RAD sequence coverage allows us to identify two discrete levels of degeneration on the Y chromosome, one of these 'evolutionary strata' coinciding with a previously inferred inverted region. Using polymorphism data from two young (<10 000 years old) ecologically diverged lake-stream population pairs, we demonstrate that recombination rate correlates with both the magnitude of allele frequency shifts between populations and levels of genetic diversity within populations. These associations reflect genome-wide heterogeneity in the influence of selection on linked sites. We further find a strong relationship between recombination rate and GC content, possibly driven by GC-biased gene conversion. Overall, we highlight that heterogeneity in recombination rate has profound consequences on genome evolution and deserves wider recognition in marker-based genomic analyses.
  Molecular Ecology 04/2013;
• Article: Molecular- and pollen-based vegetation analysis in lake sediments from central Scandinavia.

  Laura Parducci, Irina Matetovici, Sonia L Fontana, K D Bennett, Yoshihisa Suyama, James Haile, Kurt H Kjaer, Nicolaj K Larsen, Andreas D Drouzas, Eske Willerslev
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  ABSTRACT: Plant and animal biodiversity can be studied by obtaining DNA directly from the environment. This new approach in combination with the use of generic barcoding primers (metabarcoding) has been suggested as complementary or alternative to traditional biodiversity monitoring in ancient soil sediments. However, the extent to which metabarcoding truly reflects plant composition remains unclear, as does its power to identify species with no pollen or macrofossil evidence. Here, we compared pollen-based and metabarcoding approaches to explore the Holocene plant composition around two lakes in central Scandinavia. At one site, we also compared barcoding results with those obtained in earlier studies with species-specific primers. The pollen analyses revealed a larger number of taxa (46), of which the majority (78%) was not identified by metabarcoding. The metabarcoding identified 14 taxa (MTUs), but allowed identification to a lower taxonomical level. The combined analyses identified 52 taxa. The barcoding primers may favour amplification of certain taxa, as they did not detect taxa previously identified with species-specific primers. Taphonomy and selectiveness of the primers are likely the major factors influencing these results. We conclude that metabarcoding from lake sediments provides a complementary, but not an alternative, tool to pollen analysis for investigating past flora. In the absence of other fossil evidence, metabarcoding gives a local and important signal from the vegetation, but the resulting assemblages show limited capacity to detect all taxa, regardless of their abundance around the lake. We suggest that metabarcoding is followed by pollen analysis and the use of species-specific primers to provide the most comprehensive signal from the environment.
  Molecular Ecology 04/2013;
• Article: RADseq underestimates diversity and introduces genealogical biases due to nonrandom haplotype sampling.

  B Arnold, R B Corbett-Detig, D Hartl, K Bomblies
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  ABSTRACT: Reduced representation genome-sequencing approaches based on restriction digestion are enabling large-scale marker generation and facilitating genomic studies in a wide range of model and nonmodel systems. However, sampling chromosomes based on restriction digestion may introduce a bias in allele frequency estimation due to polymorphisms in restriction sites. To explore the effects of this nonrandom sampling and its sensitivity to different evolutionary parameters, we developed a coalescent-simulation framework to mimic the biased recovery of chromosomes in restriction-based short-read sequencing experiments (RADseq). We analysed simulated DNA sequence datasets and compared known values from simulations with those that would be estimated using a RADseq approach from the same samples. We compare these 'true' and 'estimated' values of commonly used summary statistics, π, θw , Tajima's D and FST . We show that loci with missing haplotypes have estimated summary statistic values that can deviate dramatically from true values and are also enriched for particular genealogical histories. These biases are sensitive to nonequilibrium demography, such as bottlenecks and population expansion. In silico digests with 102 completely sequenced Drosophila melanogaster genomes yielded results similar to our findings from coalescent simulations. Though the potential of RADseq for marker discovery and trait mapping in nonmodel systems remains undisputed, our results urge caution when applying this technique to make population genetic inferences.
  Molecular Ecology 04/2013;
• Article: Approximate Bayesian estimation of extinction rate in the Finnish Daphnia magna metapopulation.

  John D Robinson, David W Hall, John P Wares
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  ABSTRACT: Approximate Bayesian computation (ABC) is useful for parameterizing complex models in population genetics. In this study, ABC was applied to simultaneously estimate parameter values for a model of metapopulation coalescence and test two alternatives to a strict metapopulation model in the well-studied network of Daphnia magna populations in Finland. The models shared four free parameters: the subpopulation genetic diversity (θS ), the rate of gene flow among patches (4Nm), the founding population size (N0 ) and the metapopulation extinction rate (e) but differed in the distribution of extinction rates across habitat patches in the system. The three models had either a constant extinction rate in all populations (strict metapopulation), one population that was protected from local extinction (i.e. a persistent source), or habitat-specific extinction rates drawn from a distribution with specified mean and variance. Our model selection analysis favoured the model including a persistent source population over the two alternative models. Of the closest 750 000 data sets in Euclidean space, 78% were simulated under the persistent source model (estimated posterior probability = 0.769). This fraction increased to more than 85% when only the closest 150 000 data sets were considered (estimated posterior probability = 0.774). Approximate Bayesian computation was then used to estimate parameter values that might produce the observed set of summary statistics. Our analysis provided posterior distributions for e that included the point estimate obtained from previous data from the Finnish D. magna metapopulation. Our results support the use of ABC and population genetic data for testing the strict metapopulation model and parameterizing complex models of demography.
  Molecular Ecology 04/2013;
• Article: The evolutionary history of Xiphophorus fish and their sexually selected sword: a genome-wide approach using restriction site-associated DNA sequencing.

  Julia C Jones, Shaohua Fan, Paolo Franchini, Manfred Schartl, Axel Meyer
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  ABSTRACT: Next-generation sequencing (NGS) techniques are now key tools in the detection of population genomic and gene expression differences in a large array of organisms. However, so far few studies have utilized such data for phylogenetic estimations. Here, we use NGS data obtained from genome-wide restriction site-associated DNA (RAD) (∼66000 SNPs) to estimate the phylogenetic relationships among all 26 species of swordtail and platyfish (genus Xiphophorus) from Central America. Past studies, both sequence and morphology-based, have differed in their inferences of the evolutionary relationships within this genus, particularly at the species-level and among monophyletic groupings. We show that using a large number of markers throughout the genome, we are able to infer the phylogenetic relationships with unparalleled resolution for this genus. The relationships among all three major clades and species within each of them are highly resolved and consistent under maximum likelihood, Bayesian inference and maximum parsimony. However, we also highlight the current cautions with this data type and analyses. This genus exhibits a particularly interesting evolutionary history where at least two species may have arisen through hybridization events. Here, we are able to infer the paternal lineages of these putative hybrid species. Using the RAD-marker-based tree we reconstruct the evolutionary history of the sexually selected sword trait and show that it may have been present in the common ancestor of the genus. Together our results highlight the outstanding capacity that RAD sequencing data has for resolving previously problematic phylogenetic relationships, particularly among relatively closely related species.
  Molecular Ecology 04/2013;
• Article: Pervasive selection or is it…? Why are FST outliers sometimes so frequent?

  Nicolas Bierne, Denis Roze, John J Welch
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  ABSTRACT: It is now common for population geneticists to estimate FST for a large number of loci across the genome, before testing for selected loci as being outliers to the FST distribution. One surprising result of such FST scans is the often high proportion (>1% and sometimes >10%) of outliers detected, and this is often interpreted as evidence for pervasive local adaptation. In this issue of Molecular Ecolog, Fourcade et al. (2013) observe that a particularly high rate of FST outliers has often been found in river organisms, such as fishes or damselflies, despite there being no obvious reason why selection should affect a larger proportion of the genomes of these organisms. Using computer simulations, Fourcade et al. (2013) show that the strong correlation in co-ancestry produced in long onedimensional landscapes (such as rivers, valleys, peninsulas, oceanic ridges or coastlines) greatly increases the neutral variance in FST, especially when the landscape is further reticulated into fractal networks. As a consequence, outlier tests have a high rate of false positives, unless this correlation can be taken into account. Fourcade et al.'s study highlights an extreme case of the general problem, first noticed by Robertson (1975a,b) and Nei & Maruyama (1975), that correlated co-ancestry inflates the neutral variance in FST when compared to its expectation under an island model of population structure. Similar warnings about the validity of outlier tests have appeared regularly since then but have not been widely cited in the recent genomics literature. We further emphasize that FST outliers can arise in many different ways and that outlier tests are not designed for situations where the genetic architecture of local adaptation involves many loci.
  Molecular Ecology 04/2013; 22(8):2061-4.
• Article: Conclusive evidence for panmixia in the American eel.

  Jose M Pujolar
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  ABSTRACT: Eels are unique species in the biological world. The two North Atlantic eel species, the American eel (Anguilla rostrata) and the European eel (A. anguilla), occupy a broad range of habitats from the Caribbean to Greenland in the western Atlantic and from Morocco to Iceland in the eastern Atlantic, respectively. North Atlantic eels have a catadromous life cycle, spawning only in the Sargasso Sea and spending the majority of their lives in continental (fresh, brackish and coastal) waters. Despite such a wide distribution range, North Atlantic eels have been regarded as a textbook example of panmictic species. In contrast with the large amount of population genetic studies testing the panmixia hypothesis in the European eel, a relatively modest effort has been given to study the population structure of the American eel. In this issue of Molecular Ecology, C^ote et al. (2013) present the most comprehensive American eel data set to date, which includes samples of different life stages obtained throughout all its distribution range in North America. Results show a total lack of genetic differentiation among samples and provide decisive evidence for panmixia in the American eel.
  Molecular Ecology 04/2013; 22(7):1761-2.
• Article: Using genomic data to revisit an early example of reproductive character displacement in Haitian Anolis lizards.

  Shea M Lambert, Anthony J Geneva, D Luke Mahler, Richard E Glor
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  ABSTRACT: The pattern of reproductive character displacement (RCD)-in which traits associated with reproductive isolation are more different where two species occur together than where they occur in isolation-is frequently attributed to reinforcement, a process during which natural selection acting against maladaptive mating events leads to enhanced prezygotic isolation between species or incipient species. One of the first studies of RCD to include molecular genetic data was described 40 years ago in a complex of Haitian trunk anole lizards using a small number of allozyme loci. In this example, Anolis caudalis appears to experience divergence in the color and pattern of an extensible throat fan, or dewlap, in areas of contact with closely related species at the northern and southern limits of its range. However, this case study has been largely overlooked for decades; meanwhile, explanations for geographic variation in dewlap color and pattern have focused primarily on adaptation to local signalling environments. We reinvestigate this example using amplified fragment length polymorphism (AFLP) genome scans, mtDNA sequence data, information on dewlap phenotypes and GIS data on environmental variation to test the hypothesis of RCD generated by reinforcement in Haitian trunk anoles. Together, our phenotypic and genetic results are consistent with RCD at the southern and northern limits of the range of A. caudalis. We evaluate the evidence for reinforcement as the explanation for RCD in Haitian trunk anoles, consider alternative explanations and provide suggestions for future work on the relationship between dewlap variation and speciation in Haitian trunk anoles.
  Molecular Ecology 03/2013;
• Article: Microevolution in time and space: SNP analysis of historical DNA reveals dynamic signatures of selection in Atlantic cod.

  Nina O Therkildsen, Jakob Hemmer-Hansen, Thomas D Als, Douglas P Swain, M Joanne Morgan, Edward A Trippel, Stephen R Palumbi, Dorte Meldrup, Einar E Nielsen
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  ABSTRACT: Little is known about how quickly natural populations adapt to changes in their environment and how temporal and spatial variation in selection pressures interact to shape patterns of genetic diversity. We here address these issues with a series of genome scans in four overfished populations of Atlantic cod (Gadus morhua) studied over an 80-year period. Screening of >1000 gene-associated single-nucleotide polymorphisms (SNPs) identified 77 loci that showed highly elevated levels of differentiation, likely as an effect of directional selection, in either time, space or both. Exploratory analysis suggested that temporal allele frequency shifts at certain loci may correlate with local temperature variation and with life history changes suggested to be fisheries induced. Interestingly, however, largely nonoverlapping sets of loci were temporal outliers in the different populations and outliers from the 1928 to 1960 period showed almost complete stability during later decades. The contrasting microevolutionary trajectories among populations resulted in sequential shifts in spatial outliers, with no locus maintaining elevated spatial differentiation throughout the study period. Simulations of migration coupled with observations of temporally stable spatial structure at neutral loci suggest that population replacement or gene flow alone could not explain all the observed allele frequency variation. Thus, the genetic changes are likely to at least partly be driven by highly dynamic temporally and spatially varying selection. These findings have important implications for our understanding of local adaptation and evolutionary potential in high gene flow organisms and underscore the need to carefully consider all dimensions of biocomplexity for evolutionarily sustainable management.
  Molecular Ecology 03/2013;
• Article: The nematode Pristionchus pacificus as a model system for integrative studies in evolutionary biology.

  Ralf J Sommer, Angela McGaughran
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  ABSTRACT: Comprehensive studies of evolution have historically been hampered by the division among disciplines. Now, as biology moves towards an '-omics' era, it is more important than ever to tackle the evolution of function and form by considering all those research areas involved in the regulation of phenotypes. Here, we review recent attempts to establish the nematode Pristionchus pacificus as a model organism that allows integrative studies of development and evo-devo, with ecology and population genetics. Originally developed for comparative study with the nematode Caenorhabditis elegans, P. pacificus provided insight into developmental pathways including dauer formation, vulva and gonad development, chemosensation, innate immunity and neurobiology. Its subsequent discovery across a wide geographic distribution in association with scarab beetles enabled its evaluation in a biogeographic context. Development of an evolutionary field station on La Réunion Island, where P. pacificus is present in high abundance across a number of widespread habitat types, allows examination of the microfacets of evolution - processes of natural selection, adaptation and drift among populations can now be examined in this island setting. The combination of laboratory-based functional studies with fieldwork in P. pacificus has the long-term prospective to provide both proximate (mechanistic) and ultimate (evolutionary and ecological) causation and might therefore help to overcome the long-term divide between major areas in biology.
  Molecular Ecology 03/2013;
• Article: Cryptic genetic and wing pattern diversity in a mimetic Heliconius butterfly.

  R I Hill, L E Gilbert, M R Kronforst
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  ABSTRACT: Despite rampant colour pattern diversity in South America, Heliconius erato exhibits a 'postman' wing pattern throughout most of Central America. We examined genetic variation across the range of H. erato, including dense sampling in Central America, and discovered a deep genetic break, centred on the mountain range that runs through Costa Rica. This break is characterized by a novel mitochondrial lineage, which is nearly fixed in northern Central America, that branches basal to all previously described mitochondrial diversity in the species. Strong genetic differentiation also appears in Z-linked and autosomal markers, and it is further associated with a distinct, but subtle, shift in wing pattern phenotype. Comparison of clines in wing phenotype, mtDNA and nuclear markers indicate they are all centred on the mountains dividing Costa Rica, but that cline width differs among data sets. Phylogeographical analyses, accounting for this new diversity, rewrite our understanding of mimicry evolution in this system. For instance, these results suggest that H. erato originated west of the Andes, perhaps in Central America, and as many as 1 million years before its co-mimic, H. melpomene. Overall our data indicate that neutral genetic markers and colour pattern loci are congruent and converge on the same hypothesis-H. erato originated in northwest South America or Central America with a 'postman' phenotype and then radiated into the wealth of colour patterns present today.
  Molecular Ecology 03/2013;
• Article: Genetic diversity of Bartonella quintana in macaques suggests zoonotic origin of trench fever.

  Hao Li, Jie-Ying Bai, Li-Yuan Wang, Lin Zeng, Yan-Sheng Shi, Zheng-Liang Qiu, Hua-Hu Ye, Xiao-Fei Zhang, Qing-Bin Lu, Michael Kosoy, Wei Liu, Wu-Chun Cao
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  ABSTRACT: Bartonella quintana is a bacterium that causes a broad spectrum of diseases in humans including trench fever. Humans were previously considered to be the primary, if not the only, reservoir hosts for B. quintana. To identify the animal reservoir and extend our understanding of the ecological and evolutionary history of B. quintana, we examined blood samples from macaques and performed multilocus sequence typing (MLST) analysis. We demonstrated the prevalence of B. quintana infection was common in macaques from main primate centres in mainland China. Overall, 18.0% (59/328) of rhesus macaques and 12.7% (39/308) of cynomolgus macaques were found to be infected with B. quintana by blood culture and/or polymerase chain reaction. The infection was more frequently identified in juvenile and young monkeys compared with adult animals. In contrast with the relatively low level of sequence divergence of B. quintana reported in humans, our investigation revealed much higher genetic diversity in nonhuman primates. We identified 44 new nucleotide variable sites and 14 novel sequence types (STs) among the B. quintana isolates by MLST analysis. Some STs were found only in cynomolgus macaques, while some others were detected only in rhesus macaques, suggesting evidence of host-cospeciation, which were further confirmed by phylogenetic analysis and Splits decomposition analysis. Our findings suggest that trench fever may primarily be a zoonotic disease with macaques as the natural hosts.
  Molecular Ecology 03/2013;