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Discovered just before extinction? The first endemic ant from the Balearic Islands (Lasius balearicus sp. nov.) is endangered by climate change

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Abstract

AimWe analyse the taxonomic status, phylogenetic relationships, distribution and age of a newly discovered ant taxon found in the mountaintops of the island of Mallorca (Spain). We also consider the potential impact of short-term climate change on the survival of this ant and make proposals on its conservation status, risks and management.LocationBalearic Islands (Spain).Methods We used morphological, molecular and ecological evidence to assess the specific status of the potential new species. We gathered distribution data to conduct climate-based distribution modelling of present and future occupancy under several SRES emission scenarios.ResultsThe existence of a new non-cryptic species of ant (Lasius balearicus Talavera, Espadaler & Vila, sp. nov.) is described from the island of Mallorca. Its distribution was found to be extremely restricted (Serra de Tramuntana) and elevationally constrained to island summits (between 800 and 1400 m a.s.l.). Molecular dating indicated that this species diverged about 1.51 million years ago from its nearest relatives, from which it can be distinguished based on several morphological traits. Ecological niche modelling shows a dramatic reduction of areas with suitable climatic conditions under the different scenarios studied.Main conclusionsLasius balearicus represents the first endemic ant to be described in the Balearic Islands, as well as the first endemic Lasius species in the Mediterranean islands. Distribution modelling predictions, the low intraspecific genetic diversity observed, and the geographical and elevational isolation of the populations indicated a low probability for the survival of the species in the short term, thus making it a potential model to study real-time climate-based biodiversity loss. As a consequence, we strongly recommend including L. balearicus in the IUCN Red List of Threatened Species under the category ‘Endangered’. This case illustrates that a fraction of biodiversity remains unexplored even within Europe, arguably the best-studied region of the planet, and that the available time-window for us to study and protect it may be in some instances notably narrow.

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... Within its range, it is one of the most abundant of all Formicidae genera and its species are very often dominants of local myrmecofauna (Janda et al. 2004). Forty-three Lasius species are known from Europe and Mediterranean area (Borowiec 2014, Talavera et al. 2015, Seifert and Galkowski 2016, divided in five subgenera (Maruyama et al. 2008). The most numerous is the nominotypical subgenus Lasius s. str. ...
... This study was also supported by data published in recent revisions of Lasius s. str. (Seifert 1992, Talavera et al. 2015, Seifert and Galkowski 2016. ...
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Lasius tapinomoides sp. n. from Crete, Greece, is described and illustrated. It belongs to L. turcicus complex and is well characterized by very small body, extremely shallow metanotal groove and presence of suberect to erect setae on the apical part of scape. New records of Cretan members of the genus Lasius Fabricius, 1804 are provided, their checklist is updated, and the key to their determination is presented.
... nov.: COI, Wg, Top1 & 28S), while for outgroups completeness ranged from 1-7 genes (Supplementary Table S1). Most of these sequences were published previously 27,33,35,36 and accessed via GenBank (Supplementary Table S1). Sequences were aligned for individual genes using MAFFT v7.453 and Geneious v.6 software. ...
... Substitution models for each partition (gene) were selected by the program ModelFinder 39 DNA-barcoding. DNA-barcoding data analyzed in this study represent a combination of sequence data from previous publications of the authors 27,33 and public data from the Barcode of Life Data System (BOLD) 40 under the name "Lasius niger". A total of 72 DNA-barcodes were compiled to gather a dataset representing ants resembling L. niger from the Nearctic. ...
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Biological invasions are a grave threat to ecosystems. The black garden ant (Lasiusniger) is a pest species in Europe. Current literature states that L. niger occupies a disjunct native distribution in the Holarctic, however, based on recent work, we re-evaluate this distribution. The native range of L. niger is reconsidered based on phylogenetic relationships (nine mitochondrial and nuclear markers, 5670 bp), DNA-barcoding (98 Holarctic specimens), morphometry (88 Holarctic specimens, 19 different measurements) and subjective assessment of phenotype. The potential spread of this species is estimated using ecological niche modeling. Lasius niger is more closely related to other Palearctic species than to the Nearctic ants known under this name. The latter are described as a distinct species, L. ponderosae sp. nov. However, DNA-barcoding discovered established populations of L. niger in metropolitan areas in Canada (Vancouver and Halifax). We describe a morphometrical method to delineate L. ponderosae sp. nov. and L. niger. MtDNA diversity and divergence is high within L. ponderosae sp. nov., but low within L. niger. More than 1,000,000 km2 are suitable as a habitat for L. niger in North America. This case emphasizes the critical role of integrative taxonomy to detect cryptic species and identify potential biological invasions in their nascent stages.
... In order to test for monophyly, 61 outgroup species (Supporting Information Appendix S1, Table S1) were examined. For each focal species we aimed to include the closest related species in the Nearctic and Palearctic regions as outgroups based on current morphological and/ or molecular evidence (Jansen, Savolainen, & Veps€ al€ ainen, 2010;Schlick-Steiner et al., 2006;Steiner et al., 2004;Talavera, Espadaler, & Vila, 2015). Additionally, DNA-barcoding (mitochondrial gene cytochrome c oxidase I, COI) data for all available species with similar morphology was used to identify the closest relative in each region. ...
... The barcode region of the COI was sequenced for all specimens using published primers and PCR conditions (Folmer, Black, Hoeh, Lutz, & Vrijenhoek, 1994;Talavera et al., 2015). Three nuclear genes were sequenced for one of each species or major DNA-barcoding clade: wingless (Wg), topoisomerase 1 (Top1), and rDNA 28S (Abouheif & Wray, 2002;Saux, Fisher, & Spicer, 2004;Ward & Sumnicht, 2012) (see Supporting Information Appendix S1, Table S2 for sequencing coverage). ...
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Aim Continents harbour unique faunas, and only a small percentage of species naturally inhabit more than a single continent. This pattern is most evident in the insects, a morphologically small and extremely diverse group. Nevertheless, 12 species of ants have traditionally been recognized as native to both North America and Eurasia, the Holarctic region. Since intercontinental dispersal is presumably rare in ants, allopatric speciation in the absence of gene flow can be expected over evolutionary time. Here, we reassess the existence of Holarctic ant species and reconstruct their biogeographical history. Location The Holarctic. Taxon All known ant species with purportedly Holarctic distributions. Methods We reconstructed the phylogenetic relationships, biogeographical history and reassessed the taxonomic status of all known ants with Holarctic distributions using genetic data based on one mitochondrial and three nuclear genes and an ancestral area reconstruction of 310 specimens and 73 species (the 12 Holarctic species plus outgroup taxa). Results Contrary to the currently accepted hypothesis, only three ant species have Holarctic native ranges, while six taxa separate into distinct Palearctic and Nearctic species. Four species are shown to be recent introductions from Europe to North America by human activity, one of which was thought to be native. Genetic diversity is considerably higher within the North American than within European species as currently defined. Main conclusions The Formicidae have repeatedly dispersed through Beringia, during and after land bridge formation, and in both directions between the Palearctic and Nearctic regions. However, only three cold‐tolerant species crossed the Bering Strait in relatively recent time. Our results highlight the potential existence of many unknown Nearctic ant taxa. Reliance on an evolutionarily labile morphological character, erect hairs, seems to have obscured species delimitation in these ant taxa. Based on our investigation, the typical time for speciation in allopatry for ants is 2–5 Ma.
... Des de la publicació de Comín (1988), s'han anat citant noves espècies de formícids, ja sigui a causa d'introduccions humanes (Gómez i Espadaler, 2006), revisions taxonòmiques (Seifert et al., 2017), descripcions d'espècies noves per la ciència (Talavera et al., 2015) o troballes noves (Espadaler i Cagniant, 1991). Fins a dia d'avui, a Balears s'han enregistrat una seixantena d'espècies de formícids (Díaz-Calafat, en preparació). ...
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Es detecta per primer cop Camponotus barbaricus Emery 1905 a dues localitats a l’illa de Mallorca. Fins ara desconeguda, aquesta espècie de formiga passa a ser la més grossa de tota la nostra fauna. Seria estrany que una formiga d’aquestes dimensions i de comportament agressiu cap a altres artròpodes s’hagi passat per alt fins ara. Per això, sembla que la possibilitat d’una introducció recent és la més probable, tot i que no es pot descartar completament que aquesta espècie sigui en realitat autòctona de l’arxipèlag Balear. || Camponotus barbaricus Emery 1905 is recorded for the first time in two locations on the island of Mallorca. Unknown to the area until now, this ant species has become the biggest of our fauna. It would be odd that such a big species, which also shows aggressive behaviour towards other arthropods, had been overlooked up to this point. For this reason, it seems that the possibility of a recent introduction of this species on the island of Mallorca is the most likely, even though we cannot completely rule out that this species be actually autochthonous to the archipelago.
... Both studies used a combination of morphological characters and molecular data, including mitochondrial markers (COI, COII, tRNA-Leu, 16S). A more recent effort focused on the phylogeny of European species related to L. niger (Lasius s. str.) and included nuclear genes LW Rh and wg in addition to 16S and COI (Talavera et al., 2015). ...
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... Such short-range condition is unfrequently witnessed in Mediterranean ants, and may represent an element of fragility to be taken into account for conservation (e.g. Talavera et al. 2015). As the reproductive and dispersal strategies of M. sicula remain unknown at this time, it is possible to speculate that these may have contributed to confine this taxon to such a small area: low dispersal range and dependent colony foundation are associated traits in M. nipponica (Cronin et al. 2020). ...
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... All specimens from which DNA was extracted were isolated into separate tubes, used for subsequent photography and stored in > 95% ethanol thereafter. PCR reactions were carried out according to a published protocol (Talavera et al. 2015). Depending on the species, either the primer pairs LCO1490/HC02198 (Folmer et al. 1994), LCO1490/Nancy (Simon et al. 1994) or LEp1F/R (Hebert et al. 2003) yielded better results and were used for PCR reactions. ...
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A new species of Agrostis L. (A. barceloi) is described from the northern mountains of Mallorca (Balearic Islands). The new taxon belongs to sect. Agtush and is mainly related to A. alpina Scop. and A. schleicheri Jord. & Verl. on morphological grounds. However, A. barceloi differs from A. alpina by its narrowly-lanceolate inflorescence, with panicle branches erect during and after anthesis, non-scabrid leaves, and by smaller lemmas and others. The new species is distinguished from A. schleicheri by the smaller spikelets, lemma, palea, and anthers. In addition, A. barceloi is tetraploid (2n = 28), and differs cytologically from the diploid A. alpina (2n= 14) and the hexaploid A. schleicheri (2n = 56).
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Islands present both a diversity and a stability paradox. They are often highly species-poor but have considerable biological interest in terms of extraordinary endemic genera and taxonomically isolated groups. They appear to be stable, as in some cases these organisms have persisted for many millions of years, and having an oceanic climate, extreme climatic events may be comparatively rare. However, when subject to extrinsic (anthropogenic) disturbance they do not appear to be stable, but often suffer catastrophic ecological change. These apparent paradoxes are resolved when it is realized that all these features are consequences of the same island characteristics: biotic isolation and oceanicity. As a result of these two characteristics, far oceanic islands are quantitatively different from continental systems in the nature of their ecological processes, which appear to give rise to an extreme punctuated equilibrium model of evolutionary change. Endemics may be ancient relict endemics displaying prolonged stasis and persistence, or products of adaptive radiation representing rapid punctuational events. A process-based definition of a relict endemic (palaeoendemic) is one whose founding lineage (i.e. the original continental source taxon) has not left any descendents. A corollary of this definition is that the time of divergence between an endemic and its continental sister-group should predate the colonization of the island by the now endemic lineage. An example is Dicksonia arborescens which has been on St Helena for at least 9 Myrs and no longer occurs in the likely source area of Africa. These relict endemics, frequent on islands, are important as the last remnants of tranches of biodiversity that have vanished elsewhere. Island conservation strategies require an integrated understanding of both sides of the diversity and stability paradox so that both island processes and island organisms can be conserved.
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Many studies in recent years have investigated the effects of climate change on the future of biodiversity. In this review, we first examine the different possible effects of climate change that can operate at individual, population, species, community, ecosystem and biome scales, notably showing that species can respond to climate change challenges by shifting their climatic niche along three non-exclusive axes: time (e.g. phenology), space (e.g. range) and self (e.g. physiology). Then, we present the principal specificities and caveats of the most common approaches used to estimate future biodiversity at global and sub-continental scales and we synthesise their results. Finally, we highlight several challenges for future research both in theoretical and applied realms. Overall, our review shows that current estimates are very variable, depending on the method, taxonomic group, biodiversity loss metrics, spatial scales and time periods considered. Yet, the majority of models indicate alarming consequences for biodiversity, with the worst-case scenarios leading to extinction rates that would qualify as the sixth mass extinction in the history of the earth.
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Global climate change (GCC) significantly affects distributional patterns of organisms, and considerable impacts on biodiversity are predicted for the next decades. Inferred effects include large-scale range shifts towards higher altitudes and latitudes, facilitation of biological invasions and species extinctions. Alterations of biotic patterns caused by GCC have usually been predicted on the scale of taxonomically recognized morphospecies. However, the effects of climate change at the most fundamental level of biodiversity—intraspecific genetic diversity—remain elusive. Here we show that the use of morphospecies-based assessments of GCC effects will result in underestimations of the true scale of biodiversity loss. Species distribution modelling and assessments of mitochondrial DNA variability in nine montane aquatic insect species in Europe indicate that future range contractions will be accompanied by severe losses of cryptic evolutionary lineages and genetic diversity within these lineages. These losses greatly exceed those at the scale of morphospecies. We also document that the extent of range reduction may be a useful proxy when predicting losses of genetic diversity. Our results demonstrate that intraspecific patterns of genetic diversity should be considered when estimating the effects of climate change on biodiversity.