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The darting game in snails and slugs

Schilthuizen M

Trends Ecol Evol, 2005 Nov;20(11):581-4.
PMID: 16701439

Love darts are hard 'needles' that many snails and slugs use to pierce their partner during mating. In a few species, darts have been shown to play a role in sperm competition. Two new papers, by Davison et al., and Koene and Schulenburg, might further pique researchers' interest, because they show how the full potential of darts can be tapped for studies of sexual selection in hermaphrodites.
Sexual selection on land snail shell ornamentation: a hypothesis that may explain shell diversity

Schilthuizen M

BMC Evol. Biol., 2003 Jun 05;3:13.
PMID: 12791170

BACKGROUND: Many groups of land snails show great interspecific diversity in shell ornamentation, which may include spines on the shell and flanges on the aperture. Such structures have been explained as camouflage or defence, but the possibility that they might be under sexual selection has not previously been explored.
PRESENTATION OF THE HYPOTHESIS: The hypothesis that is presented consists of two parts. First, that shell ornamentation is the result of sexual selection. Second, that such sexual selection has caused the divergence in shell shape in different species.
TESTING THE HYPOTHESIS: The first part of the hypothesis may be tested by searching for sexual dimorphism in shell ornamentation in gonochoristic snails, by searching for increased variance in shell ornamentation relative to other shell traits, and by mate choice experiments using individuals with experimentally enhanced ornamentation. The second part of the hypothesis may be tested by comparing sister groups and correlating shell diversity with degree of polygamy.
IMPLICATIONS OF THE HYPOTHESIS: If the hypothesis were true, it would provide an explanation for the many cases of allopatric evolutionary radiation in snails, where shell diversity cannot be related to any niche differentiation or environmental differences.
Menno Schilthuizen

Schilthuizen M

Curr Biol, 2024 Jan 22;34(2):R40-R41.
PMID: 38262351 DOI: 10.1016/j.cub.2023.11.040

Interview with Menno Schilthuizen, who studies the evolutionary ecology of morphological diversification in related species at the Naturalis Biodiversity Center and Leiden University.
The convoluted evolution of snail chirality

Schilthuizen M, Davison A

Naturwissenschaften, 2005 Nov;92(11):504-15.
PMID: 16217668

The direction that a snail (Mollusca: Gastropoda) coils, whether dextral (right-handed) or sinistral (left-handed), originates in early development but is most easily observed in the shell form of the adult. Here, we review recent progress in understanding snail chirality from genetic, developmental and ecological perspectives. In the few species that have been characterized, chirality is determined by a single genetic locus with delayed inheritance, which means that the genotype is expressed in the mother's offspring. Although research lags behind the studies of asymmetry in the mouse and nematode, attempts to isolate the loci involved in snail chirality have begun, with the final aim of understanding how the axis of left-right asymmetry is established. In nature, most snail taxa (>90%) are dextral, but sinistrality is known from mutant individuals, populations within dextral species, entirely sinistral species, genera and even families. Ordinarily, it is expected that strong frequency-dependent selection should act against the establishment of new chiral types because the chiral minority have difficulty finding a suitable mating partner (their genitalia are on the 'wrong' side). Mixed populations should therefore not persist. Intriguingly, however, a very few land snail species, notably the subgenus Amphidromus sensu stricto, not only appear to mate randomly between different chiral types, but also have a stable, within-population chiral dimorphism, which suggests the involvement of a balancing factor. At the other end of the spectrum, in many species, different chiral types are unable to mate and so could be reproductively isolated from one another. However, while empirical data, models and simulations have indicated that chiral reversal must sometimes occur, it is rarely likely to lead to so-called 'single-gene' speciation. Nevertheless, chiral reversal could still be a contributing factor to speciation (or to divergence after speciation) when reproductive character displacement is involved. Understanding the establishment of chirality, the preponderance of dextral species and the rare instances of stable dimorphism is an important target for future research. Since the genetics of chirality have been studied in only a few pulmonate species, we also urge that more taxa, especially those from the sea, should be investigated.
Fulltext Association between shell morphology of micro-land snails (genus Plectostoma) and their predator's predatory behaviour

Liew TS, Schilthuizen M

PeerJ, 2014;2:e329.
PMID: 24749008 DOI: 10.7717/peerj.329

Predator-prey interactions are among the main ecological interactions that shape the diversity of biological form. In many cases, the evolution of the mollusc shell form is presumably driven by predation. However, the adaptive significance of several uncommon, yet striking, shell traits of land snails are still poorly known. These include the distorted coiled "tuba" and the protruded radial ribs that can be found in micro-landsnails of the genus Plectostoma. Here, we experimentally tested whether these shell traits may act as defensive adaptations against predators. We characterised and quantified the possible anti-predation behaviour and shell traits of Plectostoma snails both in terms of their properties and efficiencies in defending against the Atopos slug predatory strategies, namely, shell-apertural entry and shell-drilling. The results showed that Atopos slugs would first attack the snail by shell-apertural entry, and, should this fail, shift to the energetically more costly shell-drilling strategy. We found that the shell tuba of Plectostoma snails is an effective defensive trait against shell-apertural entry attack. None of the snail traits, such as resting behaviour, shell thickness, shell tuba shape, shell rib density and intensity can fully protect the snail from the slug's shell-drilling attack. However, these traits could increase the predation costs to the slug. Further analysis on the shell traits revealed that the lack of effectiveness in these anti-predation shell traits may be caused by a functional trade-off between shell traits under selection of two different predatory strategies.
Fulltext A Method for Quantifying, Visualising, and Analysing Gastropod Shell Form

Liew TS, Schilthuizen M

PLoS One, 2016;11(6):e0157069.
PMID: 27280463 DOI: 10.1371/journal.pone.0157069

Quantitative analysis of organismal form is an important component for almost every branch of biology. Although generally considered an easily-measurable structure, the quantification of gastropod shell form is still a challenge because many shells lack homologous structures and have a spiral form that is difficult to capture with linear measurements. In view of this, we adopt the idea of theoretical modelling of shell form, in which the shell form is the product of aperture ontogeny profiles in terms of aperture growth trajectory that is quantified as curvature and torsion, and of aperture form that is represented by size and shape. We develop a workflow for the analysis of shell forms based on the aperture ontogeny profile, starting from the procedure of data preparation (retopologising the shell model), via data acquisition (calculation of aperture growth trajectory, aperture form and ontogeny axis), and data presentation (qualitative comparison between shell forms) and ending with data analysis (quantitative comparison between shell forms). We evaluate our methods on representative shells of the genera Opisthostoma and Plectostoma, which exhibit great variability in shell form. The outcome suggests that our method is a robust, reproducible, and versatile approach for the analysis of shell form. Finally, we propose several potential applications of our methods in functional morphology, theoretical modelling, taxonomy, and evolutionary biology.
Fulltext A review of the Cholevinae from the island of Borneo (Coleoptera, Leiodidae)

Schilthuizen M, Perreau M, Njunjić I

Zookeys, 2018.
PMID: 30100790 DOI: 10.3897/zookeys.777.23212

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 Micronemadus (one species), Catops (one species), Baryodirus (one species), Ptomaphaginus (14 species), and Ptomaphaminus (13 species). The following new species are described: Micronemadussondaicus Schilthuizen & Perreau, sp. n., Ptomaphaginusgrandis Schilthuizen & Perreau, sp. n., P.louis Schilthuizen & Perreau, sp. n., P.muluensis Schilthuizen & Perreau, sp. n., and P.isabellarossellini Schilthuizen, Njunjić & Perreau, sp. n., and Ptomaphaminuskinabatanganensis Njunjić, Schilthuizen & Perreau, sp. n., P.testaceus Schilthuizen & Perreau, sp. n., P.nanus Schilthuizen & Perreau, sp. n., P.marshalli Schilthuizen & Perreau, sp. n., P.hanskii Schilthuizen & Perreau, sp. n., P.sarawacensis Schilthuizen & Perreau, sp. n., P.layangensis Schilthuizen & Perreau, sp. n., P.microphallus Schilthuizen & Perreau, sp. n., and P.alabensis Schilthuizen & Perreau, sp. n. 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.
Fulltext Additions to the knowledge of the land snails of Sabah (Malaysia, Borneo), including 48 new species

Vermeulen JJ, Liew TS, Schilthuizen M

Zookeys, 2015.
PMID: 26692803 DOI: 10.3897/zookeys.531.6097

We present reviews of the Sabah (Malaysia, on the island of Borneo) species of the following problematical genera of land snails (Mollusca, Gastropoda): Acmella and Anaglyphula (Caenogastropoda: Assimineidae); Ditropopsis (Caenogastropoda: Cyclophoridae); Microcystina (Pulmonata: Ariophantidae); Philalanka and Thysanota (Pulmonata: Endodontidae); Kaliella, Rahula, (Pulmonata: Euconulidae); Trochomorpha and Geotrochus (Pulmonata: Trochomorphidae). Next to this, we describe new species in previously revised genera, such as Diplommatina (Diplommatinidae); Georissa (Hydrocenidae); as well as some new species of genera not revised previously, such as Japonia (Cyclophoridae); Durgella and Dyakia (Ariophantidae); Amphidromus, and Trachia (Camaenidae); Paralaoma (Punctidae); Curvella (Subulinidae). All descriptions are based on the morphology of the shells. We distinguish the following 48 new species: Acmella cyrtoglyphe, Acmella umbilicata, Acmella ovoidea, Acmella nana, Acmella subcancellata, Acmella striata, and Anaglyphula sauroderma (Assimineidae); Ditropopsis davisoni, Ditropopsis trachychilus, Ditropopsis constricta, Ditropopsis tyloacron, Ditropopsis cincta, and Japonia anceps (Cyclophoridae); Diplommatina bidentata and Diplommatina tylocheilos (Diplommatinidae); Georissa leucococca and Georissa nephrostoma (Hydrocenidae); Durgella densestriata, Dyakia chlorosoma, Microcystina microrhynchus, Microcystina callifera, Microcystina striatula, Microcystina planiuscula, and Microcystina physotrochus (Ariophantidae); Amphidromus psephos and Trachia serpentinitica (Camaenidae); Philalanka tambunanensis, Philalanka obscura, Philalanka anomphala, Philalanka rugulosa, and Philalanka malimgunung (Endodontidae); Kaliella eurytrochus, Kaliella sublaxa, Kaliella phacomorpha, Kaliella punctata, Kaliella microsoma, Rahula delopleura, (Euconulidae); Paralaoma angusta (Punctidae); Curvella hadrotes (Subulinidae); Trochomorpha trachus, Trochomorpha haptoderma, Trochomorpha thelecoryphe, Geotrochus oedobasis, Geotrochus spilokeiria, Geotrochus scolops, Geotrochus kitteli, Geotrochus subscalaris, and Geotrochus meristorhachis (Trochomorphidae).
Fulltext A cybertaxonomic revision of the micro-landsnail genus Plectostoma Adam (Mollusca, Caenogastropoda, Diplommatinidae), from Peninsular Malaysia, Sumatra and Indochina

Liew TS, Vermeulen JJ, Marzuki ME, Schilthuizen M

Zookeys, 2014.
PMID: 24715783 DOI: 10.3897/zookeys.393.6717

Plectostoma is a micro land snail restricted to limestone outcrops in Southeast Asia. Plectostoma was previously classified as a subgenus of Opisthostoma because of the deviation from regular coiling in many species in both taxa. This paper is the first of a two-part revision of the genus Plectostoma, and includes all non-Borneo species. In the present paper, we examined 214 collection samples of 31 species, and obtained 62 references, 290 pictures, and 155 3D-models of 29 Plectostoma species and 51 COI sequences of 19 species. To work with such a variety of taxonomic data, and then to represent it in an integrated, scaleable and accessible manner, we adopted up-to-date cybertaxonomic tools. All the taxonomic information, such as references, classification, species descriptions, specimen images, genetic data, and distribution data, were tagged and linked with cyber tools and web servers (e.g. Lifedesks, Google Earth, and Barcoding of Life Database). We elevated Plectostoma from subgenus to genus level based on morphological, ecological and genetic evidence. We revised the existing 21 Plectostoma species and described 10 new species, namely, P. dindingensis sp. n., P. mengaburensis sp. n., P. whitteni sp. n., P. kayiani sp. n., P. davisoni sp. n., P. relauensis sp. n., P. kubuensis sp. n., P. tohchinyawi sp. n., P. tenggekensis sp. n., and P. ikanensis sp. n. All the synthesised, semantic-tagged, and linked taxonomic information is made freely and publicly available online.
Fulltext On growth and form of irregular coiled-shell of a terrestrial snail: Plectostoma concinnum (Fulton, 1901) (Mollusca: Caenogastropoda: Diplommatinidae)

Liew TS, Kok AC, Schilthuizen M, Urdy S

PeerJ, 2014;2:e383.
PMID: 24883245 DOI: 10.7717/peerj.383

The molluscan shell can be viewed as a petrified representation of the organism's ontogeny and thus can be used as a record of changes in form during growth. However, little empirical data is available on the actual growth and form of shells, as these are hard to quantify and examine simultaneously. To address these issues, we studied the growth and form of a land snail that has an irregularly coiled and heavily ornamented shell-Plectostoma concinnum. The growth data were collected in a natural growth experiment and the actual form changes of the aperture during shell ontogeny were quantified. We used an ontogeny axis that allows data of growth and form to be analysed simultaneously. Then, we examined the association between the growth and the form during three different whorl growing phases, namely, the regular coiled spire phase, the transitional constriction phase, and the distortedly-coiled tuba phase. In addition, we also explored the association between growth rate and the switching between whorl growing mode and rib growing mode. As a result, we show how the changes in the aperture ontogeny profiles in terms of aperture shape, size and growth trajectory, and the changes in growth rates, are associated with the different shell forms at different parts of the shell ontogeny. These associations suggest plausible constraints that underlie the three different shell ontogeny phases and the two different growth modes. We found that the mechanism behind the irregularly coiled-shell is the rotational changes of the animal's body and mantle edge with respect to the previously secreted shell. Overall, we propose that future study should focus on the role of the mantle and the columellar muscular system in the determination of shell form.
Population structure and coil dimorphism in a tropical land snail

Schilthuizen M, Scott BJ, Cabanban AS, Craze PG

Heredity (Edinb), 2005 Sep;95(3):216-20.
PMID: 16077741

Tree snails of the subgenus Amphidromus s. str. are unusual because of the chiral dimorphism that exists in many species, with clockwise (dextrally) and counter-clockwise (sinistrally) coiled individuals co-occurring in the same population. Given that mating in snails is normally impeded when the two partners have opposite coil, positive frequency-dependent selection should prevent such dimorphism from persisting. We test the hypothesis that a strong population structure with little movement between tree-based demes may result in the fixation of coiling morphs at a very small spatial scale, but apparent dimorphism at all larger scales. To do so, we describe the spatial structure in a Malaysian population of A. inversus (Müller, 1774) with 36% dextrals. We marked almost 700 juvenile and adult snails in a piece of forest consisting of 92 separate trees, and recorded dispersal and the proportions of dextrals and sinistrals in all trees over a 7-day period. We observed frequent movement between trees (155 events), and found that no trees had snail populations with proportions of dextrals and sinistrals that were significantly different from random. Upon recapture 1 year later, almost two-thirds of the snails had moved away from their original tree. We conclude that population structure alone cannot stabilise the coil dimorphism in Amphidromus.
Fulltext Further twists in gastropod shell evolution

Clements R, Liew TS, Vermeulen JJ, Schilthuizen M

Biol Lett, 2008 Apr 23;4(2):179-82.
PMID: 18182365 DOI: 10.1098/rsbl.2007.0602

The manner in which a gastropod shell coils has long intrigued laypersons and scientists alike. In evolutionary biology, gastropod shells are among the best-studied palaeontological and neontological objects. A gastropod shell generally exhibits logarithmic spiral growth, right-handedness and coils tightly around a single axis. Atypical shell-coiling patterns (e.g. sinistroid growth, uncoiled whorls and multiple coiling axes), however, continue to be uncovered in nature. Here, we report another coiling strategy that is not only puzzling from an evolutionary perspective, but also hitherto unknown among shelled gastropods. The terrestrial gastropod Opisthostoma vermiculum sp. nov. generates a shell with: (i) four discernable coiling axes, (ii) body whorls that thrice detach and twice reattach to preceding whorls without any reference support, and (iii) detached whorls that coil around three secondary axes in addition to their primary teleoconch axis. As the coiling strategies of individuals were found to be generally consistent throughout, this species appears to possess an unorthodox but rigorously defined set of developmental instructions. Although the evolutionary origins of O. vermiculum and its shell's functional significance can be elucidated only once fossil intermediates and live individuals are found, its bewildering morphology suggests that we still lack an understanding of relationships between form and function in certain taxonomic groups.
Fulltext Changes in richness and community composition of ectomycorrhizal fungi among altitudinal vegetation types on Mount Kinabalu in Borneo

Geml J, Morgado LN, Semenova-Nelsen TA, Schilthuizen M

New Phytol, 2017 Jul;215(1):454-468.
PMID: 28401981 DOI: 10.1111/nph.14566

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

Khalik MZ, Hendriks K, Vermeulen JJ, Schilthuizen M

Zookeys, 2018.
PMID: 30026659 DOI: 10.3897/zookeys.773.24878

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 Georissa (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 Georissa anyiensissp. n., Georissa muluensissp. n., Georissa bauensissp. n., Georissa silaburensissp. n., Georissa kinabatanganensissp. n., and Georissa sepulutensissp. n.
A review of Aulacospira Möllendorff, 1890 and Pseudostreptaxis Möllendorff, 1890 in the Philippines (Gastropoda, Pupilloidea, Hypselostomatidae)

Páll-Gergely B, Schilthuizen M, Örstan A, Auffenberg K

Zookeys, 2019;842:67-83.
PMID: 31130806 DOI: 10.3897/zookeys.842.33052

The genera Aulacospira and Pseudostreptaxis 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: Aulacospiralens Páll-Gergely & Auffenberg, sp. n., Aulacospirakrobyloides Páll-Gergely & Schilthuizen, sp. n., Pseudostreptaxisharli Páll-Gergely & Schilthuizen, sp. n.
Fulltext Inferring microevolution from museum collections and resampling: lessons learned from Cepaea

Ożgo M, Liew TS, Webster NB, Schilthuizen M

PeerJ, 2017;5:e3938.
PMID: 29093997 DOI: 10.7717/peerj.3938

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

Schilthuizen M, Seip LA, Otani S, Suhaimi J, Njunjić I

Biodivers Data J, 2017.
PMID: 29308046 DOI: 10.3897/BDJ.5.e21947

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 Clavicornaltica sabahensis sp. n. and the leiodids Colenisia chungi sp. n. and Dermatohomoeus maliauensis sp. n.
Microgeographic evolution of snail shell shape and predator behavior

Schilthuizen M, van Til A, Salverda M, Liew TS, James SS, bin Elahan B, et al.

Evolution, 2006 Sep;60(9):1851-8.
PMID: 17089969

Genetic divergence in geographically isolated populations is a prerequisite for allopatric speciation, one of the most common modes of speciation. In ecologically equivalent populations existing within a small, environmentally homogeneous area, an important role for environmentally neutral divergence is often found or inferred. We studied a species complex of conspicuously shaped Opisthostoma land snails on scattered limestone outcrops within a small area of lowland rainforest in Borneo. We used shell morphometrics, mitochondrial and nuclear DNA sequences, and marks of predation to study the factors involved in allopatric divergence. We found that a striking geographic divergence exists in shell morphology, which is partly associated with neutral genetic divergence. We also found geographic differentiation in the behavior of the snails' invertebrate predator and evidence of an evolutionary interaction between aspects of shell shape and predator behavior. Our study shows that adaptation to biotic aspects of the environment may play a more important role in allopatric speciation than previously suspected, even on a geographically very small scale.
Specimens as primary data: museums and 'open science'

Schilthuizen M, Vairappan CS, Slade EM, Mann DJ, Miller JA

Trends Ecol Evol, 2015 May;30(5):237-8.
PMID: 25813120 DOI: 10.1016/j.tree.2015.03.002
Fulltext Molecular phylogenetics and evolutionary history of the endemic land snail genus Everettia in northern Borneo

Liew TS, Marzuki ME, Schilthuizen M, Chen Y, Vermeulen JJ, Mohd-Azlan J

PeerJ, 2020;8:e9416.
PMID: 32714659 DOI: 10.7717/peerj.9416

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 Everettia 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 Everettia 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 Everettia 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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