Editorial and retrospective 2010

Abstract

The year 2009 has been another excellent period for Molecular Ecology. The impact of the journal increased from 5.17 in 2007 to 5.33 in 2008; it currently ranks sixth in impact among 124 journals listed in ISI’s Ecology category, and fifth out of 39 journals listed in ISI’s Evolutionary Biology journal category. Molecular Ecology also increased in size, with 403 articles published in 2008, making it the largest Evolutionary Biology journal and second largest Ecology journal. We also have increased the speed with which papers are published. For original and resubmitted manuscripts, we take an average of 30.4 days to make a decision (including those returned without review). For papers that are peer reviewed, we return a decision within an average of 40.6 days. Accepted manuscripts are moved to Online Early publication in 41 days (on average), with the print version appearing c. 23 days later. Thus, the time from submission to print publication of a typical paper averages 105 days or c. 3½ months. We thank our academic editors, reviewers, as well as our editorial and production staff, for their efficient processing of manuscripts. Several important policy decisions were made at our editorial board meeting this summer. These are reported below: Due to concerns about the availability and preservation of data from ecological and evolutionary studies, most of the leading journals in ecology and evolution will soon be introducing a new data archiving policy (Whitlock et al. 2010). Our current archiving policy applies only to DNA sequence data, which must be made available on GenBank or another public archive. However, the new policy will be applicable to all data-supporting results in papers published in Molecular Ecology. A more lengthy rationale for the policy can be found in Whitlock et al. (2010). Molecular Ecology’s policy will read as follows: Molecular Ecology expects, as a condition for publication, that data supporting the results in the paper should be archived in an appropriate public archive, such as GenBank, Gene Expression Omnibus, TreeBASE, Dryad, or the Knowledge Network for Biocomplexity. Data are important products of the scientific enterprise, and they should be preserved and usable for decades in the future. Authors may elect to have the data publicly available at time of publication, or, if the technology of the archive allows, may opt to embargo access to the data for a period up to a year after publication. Exceptions may be granted at the discretion of the editor, especially for sensitive information such as human subject data or the location of endangered species. Our policy will not go into force until January 2011, but in the meantime, we encourage authors to submit their data to the relevant repositories. DNA sequence data from either Sanger or next generation sequencing should continue to be archived in GenBank or another public database. Expression data should be submitted to the Gene Expression Omnibus or an equivalent database, whereas phylogenetic trees should be submitted to TreeBASE. More idiosyncratic data, such as microsatellite allele frequency data, can be archived in a more flexible digital data library such as the US National Science Foundation-sponsored Dryad archive at http://datadryad.org. Once the policy is in force in 2011, authors will be expected to archive the data supporting their results and conclusions, along with sufficient details so that a third party can interpret them correctly. As discussed by Whitlock et al. (2010), this will likely ‘require a short additional text document, with details specifying the meaning of each column in the data set. The preparation of such shareable data sets will be easiest if these files are prepared as part of the data analysis phase of the preparation of the paper, rather than after acceptance of a manuscript’. In spring 2008, we moved from an e-mail-based manuscript management system to a web-based system. An unexpected consequence of this transition has been a substantial increase in the speed of the review and publication process for all papers submitted to Molecular Ecology, essentially rendering our separate ‘Fast Track’ editorial process obsolete. Nonetheless, we feel that there is a need to accommodate high impact, short format research papers. Thus, we have replaced the Fast Track category with a new ‘From the Cover’ section. As with Fast Track, the ‘From the Cover’ section contains papers of exceptional interest to a wide audience and that address significant questions in ecology, evolution, behaviour or conservation. We will consider papers previously reviewed by other high-impact journals, with the added innovation that we will utilize all documents associated with the previous review process. The use of these review materials does not guarantee acceptance or that the manuscript will not receive external review. However, papers with largely positive reviews from leading general science journals will receive immediate consideration for publication and may not require additional review. If the authors hope to avoid additional review, they need to revise the manuscript according to reviewers’ comments and submit a cover letter that describes these changes and explains why their paper would be appropriate for publication as a Cover article in Molecular Ecology. Upon receipt, Senior Editor Bob Wayne will immediately review submissions for content and impact. Submissions that do not meet stringent standards will be returned at that stage without review, or they will be invited for resubmission as regular full papers. From the Cover manuscripts must be brief and focused, in 4000 words or less, with up to five display items (tables and figures). Accepted articles will be highlighted in the journal on the cover and in the table of contents and will frequently be featured in commentaries and press alerts. Although only a handful of papers published in Molecular Ecology involve experiments with animals, it is important these experiments be conducted properly, minimize suffering and comply with relevant regulations. Thus, we have developed the following policy: We expect that papers submitted to Molecular Ecology comply with the laws on animal experimentation in the countries where the work was conducted. All experimental procedures must be properly described and should be designed to minimize the suffering of animals. We are pleased to announce that after a brief hiatus in 2009, Molecular Ecology has two excellent special issues lined up for 2010. The first, due in February and edited by Diethard Tautz, Hans Ellegren and Detlef Weigel, is entitled ‘Next generation Molecular Ecology’. The papers in this issue offer a glimpse of the enormous potential that next-generation sequencing technology offers researchers in ecology and evolution: the chance to tackle existing problems with tremendous statistical power, and the ability to test new hypotheses unimaginable a few short years ago. The second special issue of 2010 will focus on ‘Landscape Genetics’, another rapidly developing and increasingly important field. The organizers, Lisette Waits and Victoria Sork, have brought together empirical and methodological contributions from leading workers in this area, with the aim of establishing the benchmark for research in this nascent field. We would like to extend our gratitude to the guest editors of both issues for their hard work so far, and we are delighted that they chose Molecular Ecology to showcase these cutting edge studies. A recent article in Oikos (Johnson et al. 2009c) asks the provocative question: where is the ecology in molecular ecology? The article reports on a survey of research published in Ecology, Evolution, and Molecular Ecology. Evolutionary studies are shown to be considerably more likely to employ molecular tools than are ecological studies. Also, papers published in Molecular Ecology are more likely to have an evolutionary than ecological focus, a trend we have commented on previously (Rieseberg & Smith 2002). So why do ecologists less frequently employ molecular techniques than evolutionary biologists? Johnson et al. (2009c) put forward two possible explanations. One possibility is that, for cultural reasons, the ecological sciences have been more resistant to the use of molecular tools than evolutionary biology. A second possible explanation, which we find more satisfying, is that many ecological questions can be answered without the aid of molecular techniques, whereas most evolutionary questions clearly benefit from molecular data. Nonetheless, as editors of Molecular Ecology, we have been pleasantly surprised at the many creative ways in which molecular tools are being used to address ecological questions. We also believe that the molecular biology techniques have infiltrated ecology to a greater extent than is generally recognized. Some of the ecological topics that have been addressed with molecular tools over the past year include: ecological speciation (Galindo et al. 2009; Sadedin et al. 2009), population demography (Curtis et al. 2009; Jackson et al. 2009; Liu & Ely 2009; Lundemo et al. 2009), population dynamics (Bayon et al. 2009), evolutionary ecology (Aubin-Horth & Renn 2009; Cartwright 2009; Latta 2009), behavioural ecology (Beekman et al. 2009; Berg et al. 2009; Du & Lu 2009; Johnson et al. 2009a), disease ecology (Abrego et al. 2009a; Almeida et al. 2009; Jaatinen et al. 2009; Rudge et al. 2009), macroecology (Elias et al. 2009; Parnell et al. 2009; Thomas 2009; Wilson 2009), community ecology (Abrego et al. 2009b; Carletto et al. 2009; Clare et al. 2009; Haselkorn et al. 2009), invasion ecology (Chun et al. 2009; Henry et al. 2009a; Mikheyev et al. 2009; Rollins et al. 2009), population interactions (Reisser et al. 2009), transgene escape (Pineyro-Nelson et al. 2009b; Snow 2009) and so forth. Thus, we feel that the content of Molecular Ecology is becoming more relevant to ecologists, a trend we hope will accelerate in the future. The 2009 Molecular Ecology Prize was awarded to Professor Terry Burke, of the University of Sheffield. Terry was the first chief editor of Molecular Ecology, and he pioneered the use of DNA fingerprinting methods for parentage analyses in birds. He also has made significant general contributions to our understanding of the molecular and quantitative genetics of natural populations. A biography of Terry and his contributions to molecular ecology can be found on page 23 of this issue. We regret to report that several of our longest serving and/or most distinguished editors have stepped down this year: Roger Butlin, John Dallas, Franco Widmer and John Wakeley. We thank them for their many contributions to the journal. Fortunately, several distinguished scientists have agreed to join our editorial board to serve both as replacements for our departing editors and to help handle the ever-increasing number of submissions (we expect to receive >1400 submissions this year). The new editors include Sean Rogers (University of Calgary), Rosemary Gillespie (University of California, Berkeley), Aurelie Bonin (Indiana University), Roger Thorpe (University of Bangor), Tatiana Giraud (Université Paris-Sud XI), Daniel Falush (University of Oxford), Madeleine van Oppen (Australian Institute of Marine Science) and Dany Garant (University of Sherbrooke). In addition, we will also welcome Arianne Albert as a second News and Views Editor; she will be assisting Nolan Kane with our increasingly popular Perspectives section. Welcome to all of you!! Lastly, we wish to express our gratitude to our many referees (listed below) for the donation of their time to the journal and to the discipline of molecular ecology. In recent years, we have begun publishing a retrospective (below) to discuss and highlight significant advances in molecular ecology in the previous year. This is part of a broader effort to showcase the science published in Molecular Ecology, which includes our News and Views section, cover banners, press releases and so forth. For most of the 20th century, speciation in the absence of geographic isolation (i.e. sympatric speciation) was considered to be unlikely because of the homogenizing effects of gene flow. However, recent theoretical work indicates sympatric speciation is feasible in the presence of strong disruptive natural selection and/or genetic architectures that minimize the antagonism between selection and recombination. The problem has been finding convincing empirical examples (Coyne & Orr 2004). A number of studies published in Molecular Ecology in 2009 tackled this problem. Although allopatric divergence is considered most likely in some instances (Guzik et al. 2009; McBride et al. 2009; Virgilio et al. 2009), several apparent examples of sympatric speciation are discussed, including Schizothoracine fish (Zhao et al. 2009), coral barnacles (Tsang et al. 2009), marine snails (Galindo et al. 2009; Sadedin et al. 2009) and cichlid fishes (reviewed in (Salzburger 2009). Also, early stages of sympatric divergence were characterized in Capsella (Hameister et al. 2009) and cotton–melon aphids (Carletto et al. 2009). The journal also saw a follow-up study of one of the most famous cases of sympatric speciation involving two sister species of the palm genus Howea from Lord Howe Island. Because the two palms are restricted to this very small island and are wind-pollinated, it seems likely that they diverged in sympatry (Savolainen et al. 2006). Nonetheless, this scenario has been questioned because Lord Howe Island was larger in the past, possibly affording opportunities for partial geographic isolation (Stuessy 2006). The present study showed that genetic structuring in both species is low, implying that spatial separation played a minor role, if any, in the development of reproductive isolation (Babik et al. 2009a). Likewise, little admixture was observed between the two species, indicating that the reproductive barriers are strong. These results confirm that the Howea palms likely do represent a legitimate example of speciation in the absence of significant geographic barriers to gene flow. The widespread application of molecular marker approaches to the analysis of natural populations has made it feasible to estimate the frequency and direction of hybridization involving numerous species of animals and plants. However, very few studies have attempted to explain variation in hybridization rates. A potentially important factor, first posited by the ichthyologist Carl Hubbs, is the relative abundance of the hybridizing species. Hubbs reasoned that hybridization would be most frequent when species abundances were unbalanced because a locally rare species would encounter mostly heterospecific gametes. Lepais et al. (2009) tested this conjecture by analyzing more than 2000 European oak trees with 10 microsatellite markers. Hybrids were surprisingly common, conservatively representing between 11% and 31% of genotypes within sampled populations. As predicted by Hubbs, locally dominant species were under-represented among the hybrids. Hybridization can have both negative and positive consequences for biodiversity. On the negative size, hybridization can lead to the breakdown of reproductive barriers and merger of species (so-called de-speciation). It can also lead to the extinction of rare populations through outbreeding depression or through genetic assimilation by a more widespread congener. Positive outcomes include increased rates of adaptive evolution, the formation of new races and species, and the reinforcement of reproductive barriers. Unfortunately, little is known about the relative importance of these different outcomes. However, a significant literature on the topic is being developed in Molecular Ecology and other journals, and ordering the importance of the various consequences or outcomes of hybridization is now becoming feasible. A surprise has been the very high number of instances in which hybridization appears to be contributing to adaptive evolution. For example, this year in Molecular Ecology we were able to identify six examples where hybridization was thought to be contributing to adaptation (Gagnaire et al. 2009; Gaskin et al. 2009; Hird & Sullivan 2009; Nolte et al. 2009; Pillon et al. 2009; Zidana et al. 2009), but only one case where it was a serious extinction threat (McDevitt et al. 2009). One of the most gratifying outcomes of phylogeographic studies has been the frequent discovery of cryptic species––species that are similar in morphology, but appear to represent reproductively independent lineages. Reproductive independence is usually inferred from the discovery of significant divergence in molecular markers and/or reciprocal monophyly in phylogenetic trees. Examples published in Molecular Ecology in 2009 are listed in Table 1. A major focus of Molecular Ecology since its inception has been the description and explanation of patterns of genetic variation within species. In particular, there have numerous attempts to identify and order the factors that account for spatial genetic structure. Three factors have emerged as most explanatory: habitat adaptation, geographic distance, and physical features of the environment. However, molecular ecology is a science of case studies, and conclusions require integration of information from numerous studies. In 2009, the majority of papers addressing this question in Molecular Ecology found evidence that geographic distance and physical barriers were most likely to influence patterns of gene flow and population genetic structure (Table 2), whereas habitat adaptation had a much lesser role. However, there are a number of reasons why the importance of habitat adaptation might be under-estimated. First, habitat adaptation is more difficult to quantify and its effects on spatial genetic structure are less frequently tested than geographic distance or physical barriers. Second, habitat adaptation is expected to have chromosomally local effects, whereas geographic distance and physical barriers are anticipated to have genome-wide effects. Because most studies published in Molecular Ecology sample only a small fraction of the genome, they are unlikely to detect changes in genetic variation due to local selection. In future, as more genome scans are published in the journal, we expect to see stronger evidence of a role for habitat adaptation in governing the spatial genetic structure of populations. The effects of habitat fragmentation are not always predictable, however. Although several studies (De-Lucas et al. 2009; Liu et al. 2009) found that habitat fragmentation did indeed lead to spatial genetic structure and lower variation within populations, this was not always found to be the case. Mayer et al. (2009), Mimura et al. (2009) and Purrenhage et al. (2009) found little loss in genetic variation in fragmented populations, and high medium- and long-distance dispersal. A more general survey of genetic variation in rare and endangered populations found very low genetic variation in some rare species (Ahonen et al. 2009; Boessenkool et al. 2009; Grivet et al. 2009; Johnson et al. 2009b), but surprisingly high variation in others (Duffie et al. 2009; Gonzalez-Suarez et al. 2009; Henry et al. 2009b; Shen et al. 2009; Straub & Doyle 2009). In more common, globally distributed species, high variation and little spatial genetic structure are often expected. While this is sometimes found to be the case (Nagai et al. 2009; Rosendahl et al. 2009; Shimizu-Inatsugi et al. 2009) due to high vagility and/or human-mediated dispersal, other globally distributed species show extremely high spatial genetic structure, with little gene flow between populations (Ahonen et al. 2009; Chabot & Allen 2009; Zaffarano et al. 2009). The importance of including multiple markers in any assessment of phylogeography is becoming increasingly apparent. Out of 20 such studies published in 2009 in Molecular Ecology (Table 3), only four (Cardoso & Montoya-Burgos 2009; Hoebe et al. 2009; Hunt et al. 2009; Lee & Johnson 2009) show full concordance between nuclear and cytoplasmic markers. Interestingly, a single marker may not be enough to tell the full story of even an organellar lineage; one study with five different mitochondrial markers (Xu et al. 2009) revealed important differences in the genealogies of the loci, with evidence of hybridization and recombination among mitochondrial lineages. Likely explanations for lack of concordance between nuclear and organellar markers include hybridization and mitochondrial capture (Chen et al. 2009; Nevado et al. 2009), introgression of nuclear genes but not organellar genes (Sala-Bozano et al. 2009), differences between male and female migration rates (Braaker & Heckel 2009; Makino & Tanabe 2009), and differences in the rate of evolution of nuclear and mitochondrial markers (Kempf et al. 2009). Numerous studies on invasive species have been published over the past year, with quite a clear association between the number of origins of the invasion and the amount of genetic variation present in the invasive species (Table 4). Several invasive species thought to have multiple origins did indeed have high levels of genetic variation (Brown & Stepien 2009; Chun et al. 2009; Pringle et al. 2009), in one case higher than in native populations (Zidana et al. 2009). Only a few invasive species with multiple origins have low variation (Henry et al. 2009a; Peacock et al. 2009), as did those with few origins (Mikheyev et al. 2009; Valade et al. 2009). The complex interaction between organisms and their parasites has long fascinated biologists, and many hypotheses have been advanced to explain how some individuals are able to cope with or avoid infection when others cannot. One set of loci receiving particular attention are those of the major histocompatibility complex (MHC), as these genes encode proteins responsible for mounting the adaptive immune response. The multitude of alleles found at these loci suggest strong selection for either heterozygosity or rare alleles, and hence researchers have concentrated particular effort on documenting how variation at the MHC loci varies across space and time. One surprising result published in Molecular Ecology this year found that while populations of the newt Triturus cristatus had high MHC diversity in glacial refugia populations (Romania), populations at the outer edge of the postglacial expansion (PGE) were very depauperate (Babik et al. 2009b). They also found evidence of positive selection on the MHC in Romania, raising the question of how the PGE populations had survived almost 10 000 years with minimal MHC variation. In a study on house sparrows, Loiseau et al. (2009) compared variation at the MHC with microsatellite data in spatially structured populations, and found that the MHC was much more differentiated between populations than the neutral loci, suggesting that spatially varying selection was responsible for maintaining variation. A study by Oliver et al. (2009) found evidence for the effects of drift on MHC diversity at broad spatial scales in voles, with directional and balancing selection acting more locally. A detailed molecular study on MHC-II in brown hares by Koutsogiannouli et al. (2009) also found evidence for balancing selection. Other notable studies in this area include Evans and Neff (2009), Lampert et al. (2009) and Roberts (2009). We hope that more studies of this sort will appear in the journal in the coming year. Intriguingly, there is considerable evidence that MHC loci are also involved in mate choice, but how MHC genotype affects reproductive success is currently unclear. Two papers published in 2009 shed new light on this problem (Roberts 2009). First, Eizaguirre et al. (2009) showed that female sticklebacks were more likely to choose mates with a specific MHC genotype that was more resistance to a parasite, but they generally also picked males with intermediate MHC diversity. Second, Bos et al. (2009) studied mate choice in breeding salamanders in relation to MHC genotype, finding that females produce most offspring when mated to males with similar MHC genotypes to their own. Both these studies suggest that MHC-based mate choice is highly dependent on ecological context, but that it nonetheless plays an important role in breeding decisions. A second factor potentially involved in parasite resistance and overall fitness is whole genome heterozygosity – individuals that are heterozygous at more loci (perhaps because they are less inbred) have long been thought to survive and reproduce better than more homozygous individuals. In a landmark meta-analysis, Chapman et al. (2009) surveyed the evidence for this belief, and found only weak evidence for heterozygosity–fitness correlations across many traits when using a sophisticated multivariate approach. A number of other studies addressing the relationship between individual heterozygosity and fitness-related traits have appeared in Molecular Ecology this year. For example, Pujolar et al. (2009) found no relationship between heterozygosity at 22 microsatellites and either growth rate or infection by a parasitic nematode. Similarly, Cohas et al. (2009) investigated the effect of heterozygosity on juvenile survival, adult survival and social dominance in alpine marmots, but only found a positive effect in juveniles. A study by Blanchet et al. (2009) found a contrasting result: in a population of rostrum dace infected with a fin parasite, individuals with intermediate heterozygosity had the highest parasite load. There is clear conceptual link between genome-wide heterozygosity and the level of inbreeding, and hence a considerable research effort has been directed at linking heterozygosity, inbreeding and fitness. For example, Mainguy et al. (2009) found that the offspring of mountain goats that mated with relatives were both less heterozygous and less likely to survive in their first year. One common problem with these studies is that low levels of heterozygosity may not necessarily reflect inbreeding (Ruiz-Lopez et al. 2009), and there are also pitfalls in using the same microsatellite data set to infer both parentage and the frequency of matings between relatives (Slate 2009; Wetzel & Westneat 2009). One possible solution is to use very large numbers of markers, effectively taking these studies into the genomic era. This approach was exemplified by Hagenblad et al. (2009), who used 250 microsatellites to characterize the joint effects of inbreeding and selection on the highly inbred Scandinavian wolf. They found no apparent effect of heterozygosity on fitness, but did manage to detect both balancing and directional selection in several parts of the genome. Studies focused on pathogens have become increasingly common in Molecular Ecology over the past few years, reflecting a growing effort aimed at understanding the ecology, evolution and population structure of microorganisms (Table 5). This is particularly true for newly identified invasive diseases, as these can rapidly decimate crops (Bahri et al. 2009; Crouch et al. 2009), whole taxonomic classes (e.g. Batrachochytrium dendrobatidis on amphibians: Fisher et al. 2009; Goka et al. 2009) or even threaten whole biotas within a particular geographic area (e.g. plants in California affected by Phytophthora ramorum; Goss et al. 2009; Mascheretti et al. 2009). Studies on apparently well-known and apparently stable pathogens are often equally important, as more damaging lineages can suddenly arise and spread without warning (e.g. Bayon et al. 2009). Understanding the origin and spread of these new lineages is clearly impossible in the absence of detailed information on the pathogen’s existing population structure. An ongoing major debate on the escape of transgenes has continued to unfold in the pages of Molecular Ecology. As highlighted by Snow (2009), researchers have found evidence of contamination of locally grown ‘landraces’ of maize by gene flow from modern crop cultivars in Italy (Bitocchi et al. 2009) and Mexico (Pineyro-Nelson et al. 2009a), the latter cases involving the escape of transgenes. A Comment by (Schoel & Fagan 2009) argued that the evidence for transgene escape was not definitive, and that the tests showing evidence of transgenes in Mexican landrace populations were prone to false-positives. Pineyro-Nelson et al. (2009b) replied that the tests advocated by Schoel and Fagan are prone to false-negatives, and point out that their results are backed by sequence and Southern blot data. Another interesting debate has centred on the best measure of genetic differentiation between populations. Jost (2008) proposed a new measure, D, which he argues is preferable to GST for measuring differences in allele frequencies. Heller & Siegismund (2009) performed a meta-analysis on 34 previously published studies, comparing DEST, GST and . Most importantly, GST was strongly negatively correlated with within-population genetic diversity (R2 = 0.46), a potential bias pointed out by Hedrick (2005) that complicates interpretation and can be avoided by using either DEST or . Both alternate measures were shown to be highly correlated with each other in this data set (R2 = 0.97), so may be largely interchangeable. Ryman & Leimar (2009) used simulations to show that Jost’s D is dependent on mutation rate, arguing that it cannot be easily interpreted in terms of gene flow. In his Reply, Jost (2009) points out the strengths of each measure, arguing that D is preferable for measuring allelic differentiation precisely because of its relationship to mutation rate as well as migration, but conceding that GST is preferable as a measure of migration rate itself. We owe a debt of gratitude to the large number of individuals who have contributed to the discipline of molecular e