Publications by authors named "Menno Schilthuizen"

59 Publications

The draft genome sequence of the grove snail Cepaea nemoralis.

G3 (Bethesda) 2021 02;11(2)

Evolutionary Ecology, Naturalis Biodiversity Center, Leiden 2333CR, the Netherlands.

Studies on the shell color and banding polymorphism of the grove snail Cepaea nemoralis and the sister taxon Cepaea hortensis have provided compelling evidence for the fundamental role of natural selection in promoting and maintaining intraspecific variation. More recently, Cepaea has been the focus of citizen science projects on shell color evolution in relation to climate change and urbanization. C. nemoralis is particularly useful for studies on the genetics of shell polymorphism and the evolution of "supergenes," as well as evo-devo studies of shell biomineralization, because it is relatively easily maintained in captivity. However, an absence of genomic resources for C. nemoralis has generally hindered detailed genetic and molecular investigations. We therefore generated ∼23× coverage long-read data for the ∼3.5 Gb genome, and produced a draft assembly composed of 28,537 contigs with the N50 length of 333 kb. Genome completeness, estimated by BUSCO using the metazoa dataset, was 91%. Repetitive regions cover over 77% of the genome. A total of 43,519 protein-coding genes were predicted in the assembled genome, and 97.3% of these were functionally annotated from either sequence homology or protein signature searches. This first assembled and annotated genome sequence for a helicoid snail, a large group that includes edible species, agricultural pests, and parasite hosts, will be a core resource for identifying the loci that determine the shell polymorphism, as well as in a wide range of analyses in evolutionary and developmental biology, and snail biology in general.
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http://dx.doi.org/10.1093/g3journal/jkaa071DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8022989PMC
February 2021

Evo-devo of shell colour in gastropods and bivalves.

Curr Opin Genet Dev 2020 Dec 31;69:1-5. Epub 2020 Dec 31.

Naturalis Biodiversity Center, Darwinweg 2, 2333CR Leiden, The Netherlands; Institute of Biology Leiden, Leiden University, Sylviusweg 72, 2333BE Leiden, The Netherlands. Electronic address:

Recent technical innovations are revealing surprising patterns in mollusc shell pigmentation, such as an unexpectedly modest role for melanins and rapid divergences in the mix of pigments used to achieve similar colour patterns. The elucidation of the molecular genetic basis of shell pigmentation has been slow, probably because of the high genome complexity of gastropods and bivalves. Recent work within the old field of evolutionary ecology of shell pigmentation allows a greater role for the analysis of large-geographic-scale patterns (sometimes employing citizen-science data), as well as experimental field studies. However, the field remains dominated by land snails as model organisms, while colour pattern evolution in marine gastropods and bivalves, particularly those not exposed to visual predators, remains mysterious.
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http://dx.doi.org/10.1016/j.gde.2020.11.009DOI Listing
December 2020

On the Fly: Tritrophic Associations of Bats, Bat Flies, and Fungi.

J Fungi (Basel) 2020 Dec 12;6(4). Epub 2020 Dec 12.

Research Group Mycology, Department of Biology, Ghent University, K.L. Ledeganckstraat 35, 9000 Ghent, Belgium.

Parasitism is one of the most diverse and abundant modes of life, and of great ecological and evolutionary importance. Notwithstanding, large groups of parasites remain relatively understudied. One particularly unique form of parasitism is hyperparasitism, where a parasite is parasitized itself. Bats (Chiroptera) may be parasitized by bat flies (Diptera: Hippoboscoidea), obligate blood-sucking parasites, which in turn may be parasitized by hyperparasitic fungi, Laboulbeniales (Ascomycota: Laboulbeniomycetes). In this study, we present the global tritrophic associations among species within these groups and analyze their host specificity patterns. Bats, bat flies, and Laboulbeniales fungi are shown to form complex networks, and sixteen new associations are revealed. Bat flies are highly host-specific compared to Laboulbeniales. We discuss possible future avenues of study with regard to the dispersal of the fungi, abiotic factors influencing the parasite prevalence, and ecomorphology of the bat fly parasites.
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http://dx.doi.org/10.3390/jof6040361DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7770572PMC
December 2020

Microbiome and environment explain the absence of correlations between consumers and their diet in Bornean microsnails.

Ecology 2021 02 18;102(2):e03237. Epub 2021 Jan 18.

Groningen Institute for Evolutionary Life Sciences, University of Groningen, P.O. Box 11103, Groningen, 9700 CC, The Netherlands.

Classical ecological theory posits that species partition resources such that each species occupies a unique resource niche. In general, the availability of more resources allows more species to co-occur. Thus, a strong relationship between communities of consumers and their resources is expected. However, correlations may be influenced by other layers in the food web, or by the environment. Here we show, by studying the relationship between communities of consumers (land snails) and individual diets (from seed plants), that there is in fact no direct, or at most a weak but negative, relationship. However, we found that the diversity of the individual microbiome positively correlates with both consumer community diversity and individual diet diversity in three target species. Moreover, these correlations were affected by various environmental variables, such as anthropogenic activity, habitat island size, and a possibly important nutrient source, guano runoff from nearby caves. Our results suggest that the microbiome and the environment explain the absence of correlations between diet and consumer community diversity. Hence, we advocate that microbiome inventories are routinely added to any community dietary analysis, which our study shows can be done with relatively little extra effort. Our approach presents the tools to quickly obtain an overview of the relationships between consumers and their resources. We anticipate our approach to be useful for ecologists and environmentalists studying different communities in a local food web.
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http://dx.doi.org/10.1002/ecy.3237DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7900957PMC
February 2021

Molecular phylogenetics and evolutionary history of the endemic land snail genus in northern Borneo.

PeerJ 2020 9;8:e9416. Epub 2020 Jul 9.

Institute of Biodiversity and Environmental Conservation, Universiti Malaysia Sarawak, Kota Samarahan, Sarawak, Malaysia.

Borneo has gone through dramatic changes in geology and topography from the early Eocene until the early Pliocene and experienced climatic cycling during the Pleistocene. However, how these changes have shaped the present-day patterns of high diversity and complex distribution are still poorly understood. In this study, we use integrative approaches by estimating phylogenetic relationships, divergence time, and current and past niche suitability for the Bornean endemic land snail genus to provide additional insight into the evolutionary history of this genus in northern Borneo in the light of the geological vicariance events and climatic fluctuations in the Pleistocene. Our results show that northern Borneo species belong to two deeply divergent lineages: one contains the species that inhabit high elevation at the central mountain range, while the other contains lowland species. Species diversification in these lineages has taken place before the Pliocene. Climate changes during the Pleistocene did not play a significant role in species diversification but could have shaped contemporary species distribution patterns. Our results also show that the species-rich highland habitats have acted as interglacial refugia for highland species. This study of a relatively sedentary invertebrate supports and enhances the growing understanding of the evolutionary history of Borneo. Species diversification in is caused by geological vicariance events between the early Miocene and the Pliocene, and the distribution patterns were subsequently determined by climatic fluctuations in the Pleistocene.
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http://dx.doi.org/10.7717/peerj.9416DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7354840PMC
July 2020

Imperfect and askew: A review of asymmetric genitalia in araneomorph spiders (Araneae: Araneomorphae).

PLoS One 2020 15;15(6):e0220354. Epub 2020 Jun 15.

Biodiversity Discovery group, Naturalis Biodiversity Center, Leiden, The Netherlands.

Bilateral asymmetry in the genitalia is a rare but widely dispersed phenomenon in the animal tree of life. In arthropods, occurrences vary greatly from one group to another and there seems to be no common explanation for all the independent origins. In spiders, genital asymmetry appears to be especially rare. Most known species show almost perfectly symmetrical genitals with the right and left sides being mirror images of each other. However, some examples of asymmetric genitalia have been studied and many other reports are scattered in the taxonomic literature. Based on a broad literature survey, we found several species in thirteen families with evidence of genital asymmetry, mostly expressed only in females. Our review suggests that spider genital asymmetries, although rare, are more common than previously thought and taxonomic descriptions and illustrations are a useful but not entirely reliable tool for studying them. Here we also report on directional asymmetry in the liocranid spider Teutamus politus, the first known case of morphologically asymmetric male genitals in Entelegynae spiders. Generalities, evolution and categorization of asymmetry in spiders are further discussed.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0220354PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7295216PMC
August 2020

Corrigendum to "A new parasitoid wasp, sp. n. (Braconidae, Alysiinae), from a city park in the centre of Amsterdam".

Biodivers Data J 2020 25;8:e50971. Epub 2020 Feb 25.

Naturalis, Leiden, Netherlands Naturalis Leiden Netherlands.

This corrigendum serves to recognise the contribution of Dr. Mark Lammers, who was erroneously not given authorship in the original version of the paper.
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http://dx.doi.org/10.3897/BDJ.8.e50971DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7054349PMC
February 2020

, a new species of Cyclophoridae (Gastropoda: Caenogastropoda), discovered and described on a field course to Kuala Belalong rainforest, Brunei.

Biodivers Data J 2020 20;8:e47484. Epub 2020 Feb 20.

Taxon Expeditions, Leiden, Netherlands Taxon Expeditions Leiden Netherlands.

Background: Terrestrial Caenogastropoda form an important but threatened component of the Borneo tropical rainforest malacofauna, where the group is nearly as rich in species as the Stylommatophora. They are, however, more sensitive to drought, temperature extremes and forest degradation.

New Information: On a field course at Kuala Belalong Field Studies Centre in Brunei Darussalam (Borneo), a new caenogastropod species, belonging to the genus , was discovered by the course participants. The participants decided to name the species n. sp., in honour of the climate change activist Greta Thunberg, as caenogastropod land snails, such as this species, are likely to suffer because of climate change.
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http://dx.doi.org/10.3897/BDJ.8.e47484DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7046707PMC
February 2020

A new parasitoid wasp, sp. n. (Braconidae, Alysiinae), from a city park in the centre of Amsterdam.

Biodivers Data J 2020 27;8:e49017. Epub 2020 Jan 27.

Vrije Universiteit, Amsterdam, Netherlands Vrije Universiteit Amsterdam Netherlands.

Background: The parasitic wasp genus Foerster, 1863, belongs to the large subfamily Alysiinae Leach, 1815 (Hymenoptera: Braconidae) and contains solitary or gregarious endoparasitoids of larvae of cyclorrhaphous Diptera living in decaying organic matter.

New Information: A new species, sp. n. (Braconidae, Alysiinae, Alysiini), from a city park in the centre of Amsterdam (Vondelpark) is described and illustrated. The species was discovered on a so-called taxon expedition, in which experts and citizen scientists collaborate on taxonomic projects. The finding highlights the fact that new animal species can still be discovered today, even in the busiest park of the capital of one of the best studied European countries.
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http://dx.doi.org/10.3897/BDJ.8.e49017DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6997242PMC
January 2020

Increased performance of DNA metabarcoding of macroinvertebrates by taxonomic sorting.

PLoS One 2019 16;14(12):e0226527. Epub 2019 Dec 16.

Naturalis Biodiversity Center, Leiden, the Netherlands.

DNA-based identification through the use of metabarcoding has been proposed as the next step in the monitoring of biological communities, such as those assessed under the Water Framework Directive (WFD). Advances have been made in the field of metabarcoding, but challenges remain when using complex samples. Uneven biomass distributions, preferential amplification and reference database deficiencies can all lead to discrepancies between morphological and DNA-based taxa lists. The effects of different taxonomic groups on these issues remain understudied. By metabarcoding WFD monitoring samples, we analyzed six different taxonomic groups of freshwater organisms, both separately and combined. Identifications based on metabarcoding data were compared directly to morphological assessments performed under the WFD. The diversity of taxa for both morphological and DNA-based assessments was similar, although large differences were observed in some samples. The overlap between the two taxon lists was 56.8% on average across all taxa, and was highest for Crustacea, Heteroptera, and Coleoptera, and lowest for Annelida and Mollusca. Taxonomic sorting in six basic groups before DNA extraction and amplification improved taxon recovery by 46.5%. The impact on ecological quality ratio (EQR) scoring was considerable when replacing morphology with DNA-based identifications, but there was a high correlation when only replacing a single taxonomic group with molecular data. Different taxonomic groups provide their own challenges and benefits. Some groups might benefit from a more consistent and robust method of identification. Others present difficulties in molecular processing, due to uneven biomass distributions, large genetic diversity or shortcomings of the reference database. Sorting samples into basic taxonomic groups that require little taxonomic knowledge greatly improves the recovery of taxa with metabarcoding. Current standards for EQR monitoring may not be easily replaced completely with molecular strategies, but the effectiveness of molecular methods opens up the way for a paradigm shift in biomonitoring.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0226527PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6913968PMC
April 2020

The effects of spatial and temporal replicate sampling on eDNA metabarcoding.

PeerJ 2019 26;7:e7335. Epub 2019 Jul 26.

Naturalis Biodiversity Center, Leiden, The Netherlands.

Background: The heterogeneous nature of environmental DNA (eDNA) and its effects on species detection and community composition estimates has been highlighted in several studies in the past decades. Mostly in the context of spatial distribution over large areas, in fewer occasions looking at spatial distribution within a single body of water. Temporal variation of eDNA, similarly, has mostly been studied as seasonality, observing changes over large periods of time, and often only for small groups of organisms such as fish and amphibians.

Methods: We analyzed and compared small-scale spatial and temporal variation by sampling eDNA from two small, isolated dune lakes for 20 consecutive weeks. Metabarcoding was performed on the samples using generic COI primers. Molecular operational taxonomic unit (MOTUs) were used to assess dissimilarities between spatial and temporal replicates.

Results: Our results show large differences between samples taken within one lake at one point in time, but also expose the large differences between temporal replicates, even those taken only 1 week apart. Furthermore, between-site dissimilarities showed a linear correlation with time frame, indicating that between-site differences will be inflated when samples are taken over a period of time. We also assessed the effects of PCR replicates and processing strategies on general patterns of dissimilarity between samples. While more inclusive PCR replicate strategies lead to higher richness estimations, dissimilarity patterns between samples did not significantly change.

Conclusions: We conclude that the dissimilarity of temporal replicates at a 1 week interval is comparable to that of spatial replicate samples. It increases, however, for larger time intervals, which suggests that population turnover effects can be stronger than community heterogeneity. Spatial replicates alone may not be enough for optimal recovery of taxonomic diversity, and cross-comparisons of different locations are susceptible to inflated dissimilarities when performed over larger time intervals. Many of the observed MOTUs could be classified as either phyto- or zooplankton, two groups that have gained traction in recent years as potential novel bio-indicator species. Our results, however, indicate that these groups might be susceptible to large community shifts in relatively short periods of time, highlighting the need to take temporal variations into consideration when assessing their usability as water quality indicators.
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http://dx.doi.org/10.7717/peerj.7335DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6662575PMC
July 2019

Snail shell colour evolution in urban heat islands detected via citizen science.

Commun Biol 2019 19;2:264. Epub 2019 Jul 19.

1Naturalis Biodiversity Center, 2333CR Leiden, The Netherlands.

The extreme environmental conditions that prevail in cities are known to cause selection pressures leading to adaptive changes in wild, city-dwelling, organisms (urban evolution). The urban heat island, elevated temperatures in the city centre due to a combination of generation, reflection, and trapping of heat, is one of the best recognised and most widespread urban environmental factors. Here, we use a citizen-science approach to study the effects of urban heat on genetically-determined shell colour in the land snail in the Netherlands. We use smartphone applications to obtain colour data on almost 8000 snails throughout the country. Our analysis shows that snails in urban centres are more likely to be yellow than pink, an effect predicted on the basis of thermal selection. Urban yellow snails are also more likely to carry dark bands at the underside of the shell; these bands might affect thermoregulation in yet underexplored ways.
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http://dx.doi.org/10.1038/s42003-019-0511-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6642149PMC
May 2020

A Rapid and Accurate MinION-Based Workflow for Tracking Species Biodiversity in the Field.

Genes (Basel) 2019 06 20;10(6). Epub 2019 Jun 20.

Department of Biotechnology, University of Verona, Strada Le Grazie 15, 37134 Verona, Italy.

Genetic markers (DNA barcodes) are often used to support and confirm species identification. Barcode sequences can be generated in the field using portable systems based on the Oxford Nanopore Technologies (ONT) MinION sequencer. However, to achieve a broader application, current proof-of-principle workflows for on-site barcoding analysis must be standardized to ensure a reliable and robust performance under suboptimal field conditions without increasing costs. Here, we demonstrate the implementation of a new on-site workflow for DNA extraction, PCR-based barcoding, and the generation of consensus sequences. The portable laboratory features inexpensive instruments that can be carried as hand luggage and uses standard molecular biology protocols and reagents that tolerate adverse environmental conditions. Barcodes are sequenced using MinION technology and analyzed with ONTrack, an original de novo assembly pipeline that requires as few as 1000 reads per sample. ONTrack-derived consensus barcodes have a high accuracy, ranging from 99.8 to 100%, despite the presence of homopolymer runs. The ONTrack pipeline has a user-friendly interface and returns consensus sequences in minutes. The remarkable accuracy and low computational demand of the ONTrack pipeline, together with the inexpensive equipment and simple protocols, make the proposed workflow particularly suitable for tracking species under field conditions.
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http://dx.doi.org/10.3390/genes10060468DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6627956PMC
June 2019

A review of Möllendorff, 1890 and Möllendorff, 1890 in the Philippines (Gastropoda, Pupilloidea, Hypselostomatidae).

Zookeys 2019 7;842:67-83. Epub 2019 May 7.

Florida Museum of Natural History, University of Florida, Gainesville, Florida, USA University of Florida Gainesville United States of America.

The genera and of the Philippines are revised based on the collections of the Senckenberg Forschungsinstitut und Naturmuseum (Frankfurt am Main, Germany), the Florida Museum of Natural History (USA), and recently collected material. Three new species are described: Páll-Gergely & Auffenberg, , Páll-Gergely & Schilthuizen, , Páll-Gergely & Schilthuizen,
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http://dx.doi.org/10.3897/zookeys.842.33052DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6517363PMC
May 2019

Conchological and molecular analysis of the "non-scaly" Bornean with descriptions of three new species (Gastropoda, Neritimorpha, Hydrocenidae).

Zookeys 2019 17;840:35-86. Epub 2019 Apr 17.

Naturalis Biodiversity Center, Vondellaan 55, 2332 AA Leiden, The Netherlands Universiti Malaysia Sarawak Kota Samarahan Malaysia.

The Bornean representatives of the genus (Hydrocenidae) have small, dextral, conical, calcareous shells consisting of ca. three teleoconch whorls. Our recent study on the of Malaysian Borneo has revealed high intra- and inter-specific variation in the "scaly" group (a group of species with striking scale-like surface sculpture). The present study on the "non-scaly" is the continuation of the species revision for the genus. The "non-scaly" species are also diverse in shell sculptures. This informal group comprises with subtle spiral and/or radial sculpture. The combination of detailed conchological assessment and molecular analyses provides clear distinctions for each of the species. Conchological, molecular, and biogeographic details are presented for 16 species of "non-scaly" . Three of these are new to science, namely , , and
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http://dx.doi.org/10.3897/zookeys.840.33326DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6482118PMC
April 2019

A new species of (Coleoptera: Chrysomelidae), discovered and described on a field course to Kuala Belalong, Brunei.

Biodivers Data J 2019 31(7):e32555. Epub 2019 Jan 31.

Taxon Expeditions, Leiden, Netherlands Taxon Expeditions Leiden Netherlands.

Background: is a genus of very small flea beetles living in the leaf litter layer of Asian forests, easily sampled with Winkler extraction. The genus is presumably very rich in species, but their taxonomy is hampered by their small size and morphological uniformity.

New Information: On a 'taxon expedition'-style field course at Kuala Belalong Field Studies Centre in Brunei Darussalam (Borneo), a new species, n. sp., was discovered and taxonomically treated by the course participants. We also present the first DNA barcodes for the genus.
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http://dx.doi.org/10.3897/BDJ.7.e32555DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6367309PMC
January 2019

A review of the Cholevinae from the island of Borneo (Coleoptera, Leiodidae).

Zookeys 2018 30(777):57-108. Epub 2018 Jul 30.

Naturalis Biodiversity Center, Darwinweg 2, 2333CR Leiden, The Netherlands Naturalis Biodiversity Center Leiden Netherlands.

The available knowledge of the round fungus beetle subfamily Cholevinae (Leiodidae) from the island of Borneo is reviewed, and the results of newly studied material presented. The currently known 30 species (of which 14 are newly described herein) represent the genera (one species), (one species), (one species), (14 species), and (13 species). The following new species are described: Schilthuizen & Perreau, , Schilthuizen & Perreau, , Schilthuizen & Perreau, , Schilthuizen & Perreau, , and Schilthuizen, Njunjić & Perreau, , and Njunjić, Schilthuizen & Perreau, , Schilthuizen & Perreau, , Schilthuizen & Perreau, , Schilthuizen & Perreau, , Schilthuizen & Perreau, , Schilthuizen & Perreau, , Schilthuizen & Perreau, , Schilthuizen & Perreau, , and Schilthuizen & Perreau, It is expected that the cholevine biodiversity of Borneo is still far from completely known. Nonetheless, provisional identification keys to all species known so far are presented.
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http://dx.doi.org/10.3897/zookeys.777.23212DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6079114PMC
July 2018

A molecular and conchological dissection of the "scaly" of Malaysian Borneo (Gastropoda, Neritimorpha, Hydrocenidae).

Zookeys 2018 9(773):1-55. Epub 2018 Jul 9.

Naturalis Biodiversity Center, Vondellaan 55, 2332 AA Leiden, The Netherlands.

The Bornean hydrocenids have so far been understudied compared to other non-pulmonate snails in this region. In the present study, we review a first group of minute land snail species belonging to the genus (Gastropoda, Hydrocenidae) from Malaysian Borneo. This group is restricted to the species with conspicuous scale-like sculpture on the shell. Based on materials from recent fieldwork, museums, and personal collections, Malaysian Borneo hydrocenids are more complex and diverse in shell characters than previously anticipated. Here, a molecular, conchological, and biogeographic study of this "scaly group" is presented. We recognise 13 species of which six are new to science, namely , , , , , and
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http://dx.doi.org/10.3897/zookeys.773.24878DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6048177PMC
July 2018

Comprehensive evolutionary analysis of the Anthroherpon radiation (Coleoptera, Leiodidae, Leptodirini).

PLoS One 2018 8;13(6):e0198367. Epub 2018 Jun 8.

Institut de Systématique, Évolution et Biodiversité, ISYEB - UMR 7205 CNRS, MNHN, UPMC, EPHE, Muséum national d'Histoire naturelle, Sorbonne Universités, Paris, France.

The genus Anthroherpon Reitter, 1889 exhibits the most pronounced troglomorphic characters among Coleoptera, and represents one of the most spectacular radiations of subterranean beetles. However, radiation, diversification, and biogeography of this genus have never been studied in a phylogenetic context. This study provides a comprehensive evolutionary analysis of the Anthroherpon radiation, using a dated molecular phylogeny as a framework for understanding Anthroherpon diversification, reconstructing the ancestral range, and exploring troglomorphic diversity. Based on 16 species and 22 subspecies, i.e. the majority of Anthroherpon diversity, we reconstructed the phylogeny using Bayesian analysis of six loci, both mitochondrial and nuclear, comprising a total of 4143 nucleotides. In parallel, a morphometric analysis was carried out with 79 landmarks on the body that were subjected to geometric morphometrics. We optimized morphometric features to phylogeny, in order to recognize the way troglomorphy was expressed in different clades of the tree, and did character evolution analyses. Finally, we reconstructed the ancestral range of the genus using BioGeoBEARS. Besides further elucidating the suprageneric classification of the East-Mediterranean Leptodirini, our main findings also show that Anthroherpon dates back to the Early Miocene (ca. 22 MYA) and that the genus diversified entirely underground. Biogeographic reconstruction of the ancestral range shows the origin of the genus in the area comprising three high mountains in western Montenegro, which is in the accordance with the available data on the paleogeography of the Balkan Peninsula. Character evolution analysis indicates that troglomorphic morphometric traits in Anthroherpon mostly evolve neutrally but may diverge adaptively under syntopic competition.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0198367PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5993249PMC
December 2018

Comparative genomics of the nonlegume reveals insights into evolution of nitrogen-fixing rhizobium symbioses.

Proc Natl Acad Sci U S A 2018 05 1;115(20):E4700-E4709. Epub 2018 May 1.

Bioinformatics Group, Department of Plant Sciences, Wageningen University, 6708 PB, Wageningen, The Netherlands.

Nodules harboring nitrogen-fixing rhizobia are a well-known trait of legumes, but nodules also occur in other plant lineages, with rhizobia or the actinomycete as microsymbiont. It is generally assumed that nodulation evolved independently multiple times. However, molecular-genetic support for this hypothesis is lacking, as the genetic changes underlying nodule evolution remain elusive. We conducted genetic and comparative genomics studies by using species (Cannabaceae), the only nonlegumes that can establish nitrogen-fixing nodules with rhizobium. Intergeneric crosses between and its nonnodulating relative demonstrated that nodule organogenesis, but not intracellular infection, is a dominant genetic trait. Comparative transcriptomics of and the legume revealed utilization of at least 290 orthologous symbiosis genes in nodules. Among these are key genes that, in legumes, are essential for nodulation, including () and (). Comparative analysis of genomes from three species and related nonnodulating plant species show evidence of parallel loss in nonnodulating species of putative orthologs of , , and Parallel loss of these symbiosis genes indicates that these nonnodulating lineages lost the potential to nodulate. Taken together, our results challenge the view that nodulation evolved in parallel and raises the possibility that nodulation originated ∼100 Mya in a common ancestor of all nodulating plant species, but was subsequently lost in many descendant lineages. This will have profound implications for translational approaches aimed at engineering nitrogen-fixing nodules in crop plants.
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http://dx.doi.org/10.1073/pnas.1721395115DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5960304PMC
May 2018

Dispatch from the field II: the mystery of the red and blue male (Araneae, Tetragnathidae, ).

Biodivers Data J 2018 3(6):e24777. Epub 2018 Apr 3.

Danau Girang Field Centre, Sabah, Malaysia.

Background: Males of are difficult to associate with conspecific females, and sex-matching errors may persist in the taxonomic literature. Recommended best practices for definitive sex matching in this genus suggest finding a male in the web of a female, or better yet, mating pairs.

New Information: A male was observed hanging on a frame line of the web of a female , a species for which the male was previously undescribed. This occurred during a tropical ecology field course held at the Danau Girang Field Centre in Sabah, Malaysia. A taxonomic description was completed as a course activity.
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http://dx.doi.org/10.3897/BDJ.6.e24777DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5904518PMC
April 2018

Three new minute leaf litter beetles discovered by citizen scientists in Maliau Basin, Malaysian Borneo (Coleoptera: Leiodidae, Chrysomelidae).

Biodivers Data J 2017 4(5):e21947. Epub 2017 Dec 4.

Taxon Expeditions, Leiden, Netherlands.

Background: We coin the term "taxon expeditions" for citizen scientists' field courses to carry out publishable taxonomic work in close association with trained taxonomists.

New Information: During the first-ever taxon expedition, in Maliau Basin Studies Centre, Sabah, Malaysian Borneo, the participants sampled leaf litter beetles from lowland dipterocarp forest using the Winkler apparatus. The collected material proved to contain at least three undescribed species of small-bodied (ca. 1 mm long) hemispherical litter-dwelling Coleoptera. As part of the field course work, taxonomic descriptions were prepared for the chrysomelid sp. n. and the leiodids sp. n. and sp. n.
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http://dx.doi.org/10.3897/BDJ.5.e21947DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5740419PMC
December 2017

Inferring microevolution from museum collections and resampling: lessons learned from .

PeerJ 2017 27;5:e3938. Epub 2017 Oct 27.

Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah, Kota Kinabalu, Sabah, Malaysia.

Natural history collections are an important and largely untapped source of long-term data on evolutionary changes in wild populations. Here, we utilize three large geo-referenced sets of samples of the common European land-snail stored in the collection of Naturalis Biodiversity Center in Leiden, the Netherlands. Resampling of these populations allowed us to gain insight into changes occurring over 95, 69, and 50 years. is polymorphic for the colour and banding of the shell; the mode of inheritance of these patterns is known, and the polymorphism is under both thermal and predatory selection. At two sites the general direction of changes was towards lighter shells (yellow and less heavily banded), which is consistent with predictions based on on-going climatic change. At one site no directional changes were detected. At all sites there were significant shifts in morph frequencies between years, and our study contributes to the recognition that short-term changes in the states of populations often exceed long-term trends. Our interpretation was limited by the few time points available in the studied collections. We therefore stress the need for natural history collections to routinely collect large samples of common species, to allow much more reliable hind-casting of evolutionary responses to environmental change.
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http://dx.doi.org/10.7717/peerj.3938DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5661451PMC
October 2017

Candidate genes for shell colour polymorphism in .

PeerJ 2017 18;5:e3715. Epub 2017 Sep 18.

Department of Ecological Science, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands.

The characteristic ground colour and banding patterns on shells of the land snail form a classic study system for genetics and adaptation as it varies widely between individuals. We use RNAseq analysis to identify candidate genes underlying this polymorphism. We sequenced cDNA from the foot and the mantle (the shell-producing tissue) of four individuals of two phenotypes and produced a transcriptome of 147,397 contigs. Differential expression analysis identified a set of 1,961 transcripts that were upregulated in mantle tissue. Sequence variant analysis resulted in a set of 2,592 transcripts with single nucleotide polymorphisms (SNPs) that differed consistently between the phenotypes. Inspection of the overlap between the differential expression analysis and SNP analysis yielded a set of 197 candidate transcripts, of which 38 were annotated. Four of these transcripts are thought to be involved in production of the shell's nacreous layer. Comparison with morph-associated Restriction-site Associated DNA (RAD)-tags from a published study yielded eight transcripts that were annotated as metallothionein, a protein that is thought to inhibit the production of melanin in melanocytes. These results thus provide an excellent starting point for the elucidation of the genetic regulation of the shell colour polymorphism.
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http://dx.doi.org/10.7717/peerj.3715DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5607911PMC
September 2017

Postmating sexual selection and the enigmatic jawed genitalia of .

Biol Open 2017 Jul 15;6(7):1008-1012. Epub 2017 Jul 15.

Department of Ecology and Genetics, Animal Ecology, Evolutionsbiologiskt Centrum EBC, Norbyvägen 18 D, SE-752 36 Uppsala, Uppsala University, Sweden.

Insect genitalia exhibit rapid divergent evolution. Truly extraordinary structures have evolved in some groups, presumably as a result of postmating sexual selection. To increase our understanding of this phenomenon, we studied the function of one such structure. The male genitalia of (Coleoptera: Bruchinae) contain a pair of jaw-like structures with unknown function. Here, we used phenotypic engineering to ablate the teeth on these jaws. We then experimentally assessed the effects of ablation of the genital jaws on mating duration, ejaculate weight, male fertilization success and female fecundity, using a double-mating experimental design. We predicted that copulatory wounding in females should be positively related to male fertilization success; however, we found no significant correlation between genital tract scarring in females and male fertilization success. Male fertilization success was, however, positively related to the amount of ejaculate transferred by males and negatively related to female ejaculate dumping. Ablation of male genital jaws did not affect male relative fertilization success but resulted in a reduction in female egg production. Our results suggest that postmating sexual selection in males indeed favors these genital jaws, not primarily through an elevated relative success in sperm competition but by increasing female egg production.
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http://dx.doi.org/10.1242/bio.025684DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5550917PMC
July 2017

Changes in richness and community composition of ectomycorrhizal fungi among altitudinal vegetation types on Mount Kinabalu in Borneo.

New Phytol 2017 Jul 12;215(1):454-468. Epub 2017 Apr 12.

Biodiversity Dynamics Research Group, Naturalis Biodiversity Center, Vondellaan 55, PO Box 9517, 2300 RA, Leiden, the Netherlands.

The distribution patterns of tropical ectomycorrhizal (ECM) fungi along altitudinal gradients remain largely unknown. Furthermore, despite being an iconic site for biodiversity research, virtually nothing is known about the diversity and spatial patterns of fungi on Mt Kinabalu and neighbouring mountain ranges. We carried out deep DNA sequencing of soil samples collected between 425 and 4000 m above sea level to compare richness and community composition of ECM fungi among altitudinal forest types in Borneo. In addition, we tested whether the observed patterns are driven by habitat or by geometric effect of overlapping ranges of species (mid-domain effect). Community composition of ECM fungi was strongly correlated with elevation. In most genera, richness peaked in the mid-elevation montane forest zone, with the exception of tomentelloid fungi, which showed monotonal decrease in richness with increasing altitude. Richness in lower-mid- and mid-elevations was significantly greater than predicted under the mid-domain effect model. We provide the first insight into the composition of ECM fungal communities and their strong altitudinal turnover in Borneo. The high richness and restricted distribution of many ECM fungi in the montane forests suggest that mid-elevation peak richness is primarily driven by environmental characteristics of this habitat and not by the mid-domain effect.
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http://dx.doi.org/10.1111/nph.14566DOI Listing
July 2017

The database of the PREDICTS (Projecting Responses of Ecological Diversity In Changing Terrestrial Systems) project.

Ecol Evol 2017 01 16;7(1):145-188. Epub 2016 Dec 16.

Imperial College London South Kensington London UK.

The PREDICTS project-Projecting Responses of Ecological Diversity In Changing Terrestrial Systems (www.predicts.org.uk)-has collated from published studies a large, reasonably representative database of comparable samples of biodiversity from multiple sites that differ in the nature or intensity of human impacts relating to land use. We have used this evidence base to develop global and regional statistical models of how local biodiversity responds to these measures. We describe and make freely available this 2016 release of the database, containing more than 3.2 million records sampled at over 26,000 locations and representing over 47,000 species. We outline how the database can help in answering a range of questions in ecology and conservation biology. To our knowledge, this is the largest and most geographically and taxonomically representative database of spatial comparisons of biodiversity that has been collated to date; it will be useful to researchers and international efforts wishing to model and understand the global status of biodiversity.
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http://dx.doi.org/10.1002/ece3.2579DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5215197PMC
January 2017

A review and meta-analysis of the enemy release hypothesis in plant-herbivorous insect systems.

PeerJ 2016 21;4:e2778. Epub 2016 Dec 21.

Groningen Institute for Evolutionary Life Sciences, University of Groningen , Groningen , the Netherlands.

A suggested mechanism for the success of introduced non-native species is the enemy release hypothesis (ERH). Many studies have tested the predictions of the ERH using the community approach (native and non-native species studied in the same habitat) or the biogeographical approach (species studied in their native and non-native range), but results are highly variable, possibly due to large variety of study systems incorporated. We therefore focused on one specific system: plants and their herbivorous insects. We performed a systematic review and compiled a large number (68) of datasets from studies comparing herbivorous insects on native and non-native plants using the community or biogeographical approach. We performed a meta-analysis to test the predictions from the ERH for insect diversity (number of species), insect load (number of individuals) and level of herbivory for both the community and biogeographical approach. For both the community and biogeographical approach insect diversity was significantly higher on native than on non-native plants. Insect load tended to be higher on native than non-native plants at the community approach only. Herbivory was not different between native and non-native plants at the community approach, while there was too little data available for testing the biogeographical approach. Our meta-analysis generally supports the predictions from the ERH for both the community and biogeographical approach, but also shows that the outcome is importantly determined by the response measured and approach applied. So far, very few studies apply both approaches simultaneously in a reciprocal manner while this is arguably the best way for testing the ERH.
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http://dx.doi.org/10.7717/peerj.2778DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5180588PMC
December 2016

The evolution of asymmetric genitalia in Coleoptera.

Philos Trans R Soc Lond B Biol Sci 2016 12;371(1710)

Endless Forms Group, Naturalis Biodiversity Center, Darwinweg 2, 2333CR Leiden, The Netherlands.

The evolution of asymmetry in male genitalia is a pervasive and recurrent phenomenon across almost the entire animal kingdom. Although in some taxa the asymmetry may be a response to the evolution of one-sided, male-above copulation from a more ancestral female-above condition, in other taxa, such as Mammalia and Coleoptera, this explanation appears insufficient. We carried out an informal assessment of genital asymmetry across the Coleoptera and found that male genital asymmetry is present in 43% of all beetle families, and at all within-family taxonomic levels. In the most diverse group, Cucujiformia, however, genital asymmetry is comparatively rare. We also reconstructed the phylogeny of the leiodid tribe Cholevini, and mapped aspects of genital asymmetry on the tree, revealing that endophallus sclerites, endophallus, median lobe and parameres are, in a nested fashion, increasingly unlikely to have evolved asymmetry. We interpret these results in the light of cryptic female choice versus sexually antagonistic coevolution and advocate further ways in which the phenomenon may be better understood.This article is part of the themed issue 'Provocative questions in left-right asymmetry'.
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http://dx.doi.org/10.1098/rstb.2015.0400DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5104500PMC
December 2016

Drosophila pachea asymmetric lobes are part of a grasping device and stabilize one-sided mating.

BMC Evol Biol 2016 Sep 1;16:176. Epub 2016 Sep 1.

Team "Évolution des drosophiles", Institut Jacques Monod, CNRS, UMR 7592, Université Paris Diderot, Sorbonne Paris Cité, 15 rue Hélène Brion, 75013, Paris, France.

Background: Multiple animal species exhibit morphological asymmetries in male genitalia. In insects, left-right genital asymmetries evolved many times independently and have been proposed to appear in response to changes in mating position. However, little is known about the relationship between mating position and the interaction of male and female genitalia during mating, and functional analyses of asymmetric morphologies in genitalia are virtually non-existent. We investigated the relationship between mating position, asymmetric genital morphology and genital coupling in the fruit fly Drosophila pachea, in which males possess an asymmetric pair of external genital lobes and mate in an unusual right-sided position on top of the female.

Results: We examined D. pachea copulation by video recording and by scanning electron microscopy of genital complexes. We observed that the interlocking of male and female genital organs in D. pachea is remarkably different from genital coupling in the well-studied D. melanogaster. In D. pachea, the female oviscapt valves are asymmetrically twisted during copulation. The male's asymmetric lobes tightly grasp the female's abdomen in an asymmetric 'locking' position, with the left and right lobes contacting different female structures. The male anal plates, which grasp the female genitalia in D. melanogaster, do not contact the female in D. pachea. Experimental lobe amputation by micro-surgery and laser-ablation of lobe bristles led to aberrant coupling of genitalia and variable mating positions, in which the male was tilted towards the right side of the female.

Conclusion: We describe, for the first time, how the mating position depends on coupling of male and female genitalia in a species with asymmetric genitalia and one-sided mating position. Our results show that D. pachea asymmetric epandrial lobes do not act as a compensatory mechanism for the change from symmetric to one-sided mating position that occurred during evolution of D. pachea's ancestors, but as holding devices with distinct specialized functions on the left and right sides.
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http://dx.doi.org/10.1186/s12862-016-0747-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5009675PMC
September 2016
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