Thermal niche evolution and geographical range expansion in a species complex of western Mediterranean diving beetles

[Background] Species thermal requirements are one of the principal determinants of their ecology and biogeography, although our understanding of the interplay between these factors is limited by the paucity of integrative empirical studies. Here we use empirically collected thermal tolerance data in combination with molecular phylogenetics/phylogeography and ecological niche modelling to study the evolution of a clade of three western Mediterranean diving beetles, the Agabus brunneus complex.[Results] The preferred mitochondrial DNA topology recovered A. ramblae (North Africa, east Iberia and Balearic islands) as paraphyletic, with A. brunneus (widespread in the southwestern Mediterranean) and A. rufulus (Corsica and Sardinia) nested within it, with an estimated origin between 0.60-0.25 Ma. All three species were, however, recovered as monophyletic using nuclear DNA markers. A Bayesian skyline plot suggested demographic expansion in the clade at the onset of the last glacial cycle. The species thermal tolerances differ significantly, with A. brunneus able to tolerate lower temperatures than the other taxa. The climatic niche of the three species also differs, with A. ramblae occupying more arid and seasonal areas, with a higher minimum temperature in the coldest month. The estimated potential distribution for both A. brunneus and A. ramblae was most restricted in the last interglacial, becoming increasingly wider through the last glacial and the Holocene.[Conclusions] The A. brunneus complex diversified in the late Pleistocene, most likely in south Iberia after colonization from Morocco. Insular forms did not differentiate substantially in morphology or ecology, but A. brunneus evolved a wider tolerance to cold, which appeared to have facilitated its geographic expansion. Both A. brunneus and A. ramblae expanded their ranges during the last glacial, although they have not occupied areas beyond their LGM potential distribution except for isolated populations of A. brunneus in France and England. On the islands and possibly Tunisia secondary contact between A. brunneus and A. ramblae or A. rufulus has resulted in introgression. Our work highlights the complex dynamics of speciation and range expansions within southern areas during the last glacial cycle, and points to the often neglected role of North Africa as a source of European biodiversity.This work was supported by an FPI grant to AH-G and projects CGL2007-61665 and CGL2010-15755 from the Spanish government to IR. We acknowledge support of the publication fee by the CSIC Open Access Publication Support Initiative through its Unit of Information Resources for Research (URICI).Peer reviewe

Evolution of thermal tolerance and size of the geographic range in closely related species of water beetles

[spa] Esta tesis parte del estudio de un grupo de especies de escarabajos acuáticos (Agabus brunneus complex) que poseen diferencias importantes en el tamaño de sus rangos geográficos, contando con una especie insular (A. rufulus), una continental de rango restringido (A. ramblae) y una continental de rango amplio (A. brunneus) para estudiar los factores implicados en esas diferencias. Este complejo de especies diversificó a finales del Pleistoceno en la península ibérica posiblemente tras la colonización de A. ramblae desde Marruecos. Una de las especies resultantes A. brunneus en algún momento de la diversificación desarrolló la capacidad de resistencia a bajas temperaturas lo que le facilitó el poder extender su rango hacia climas más fríos. Se empleó la proteómica de poblaciones para analizar la respuesta de varias poblaciones de A. brunneus y A. ramblae frente a temperaturas que pueden experimentar en la naturaleza. Al estudiar la variabilidad a distintos niveles entre dos poblaciones naturales de A. ramblae obtuvimos una buena reproducibilidad de nuestros experimentos. Al analizar de forma global dos poblaciones para cada especie (Marruecos y península ibérica para ambas) descubrimos que la diversificación de la filogenia ha ido acompañada de cambios en la respuesta a nivel de expresión proteínica. La mayoría de las proteínas identificadas están relacionadas con el metabolismo energético y con proteínas del estrés, estas últimas se expresan diferencialmente entre las dos especies analizadas, indicando una diferente respuesta al estrés térmico. El presente trabajo abre la posibilidad de realizar este tipo de experimentos empleando poblaciones naturales de especies no modelo y demuestra que la respuesta frente al estrés de un factor ambiental, en este caso la temperatura, puede recuperarse empleando para ello la proteómica. Así mismo las diferencias en el tamaño del rango pueden ir acompañadas de la adquisición de distinta capacidad de respuesta frente al estrés térmico[eng] This thesis studies a group of aquatic beetles (Agabus brunneus complex) that present important differences in the size of their geographic ranges. This complex is composed by an insular species (A. rufulus), a continental species with restricted range (A. ramblae) and another continental species (A. brunneus) that posses a wide range of distribution (A. brunneus) with the aim of study the factors implied in those differences. For this purpose we integrated the phylogeny/ phylogeography of the group and the evolution of the ecological niche together with morphological study and thermal tolerance of species. This complex of species diversified at the end of Pleistocene in Iberian Peninsula probably after the colonization of A. ramblae from Morocco. One of the resultant species (A. brunneus) at some point of the diversification acquired the ability to resist colder temperatures and was able to disperse to colder climates. To understand range variability from another perspective we used population proteomics to analyse the response of several populations for A. ramblae and A. bruneus facing temperatures that they might experience on field. We decided to analyse the variability at several levels in two populations of (A. ramblae) when working with natural populations obtaining satisfactory results for the reproducibility of our experimental methodology. When we analysed globally two populations for each species (one from Morocco and one from Iberian peninsula for each) we saw that the diversification observed in the phylogeny was encompassed with changes at the proteomic response. The more common proteins identified belong to energetic metabolism and stress proteins. The latter were detected to express differentially between the two species studied, showing a different response to thermal stress. This work address the possibility of employing population proteomics in natural populations of non-model species and being able of recovering the stress response facing an environmental factor like temperature. We show as well that differences in range size can be encompassing with the acquisition of capacity to face thermal stress

Evolución de la tolerancia térmica y el tamaño del rango geográfico en especies hermanas de escarabajos acuáticos

Memoria presentada por Amparo Hidalgo Galiana para optar al título de Doctor.-- Tutor: Julio Rozas LiraPeer reviewe

Late Miocene diversification of the genus Hydrochus (Coleoptera, Hydrochidae) in the west Mediterranean area

9 páginas, 4 figuras, 3 tablas.We provide a reconstruction of the phylogenetic relationships, the geographical and temporal origin, and the mode of diversification of the Mediterranean species of the aquatic beetle family Hydrochidae (Coleoptera, Hydrophiloidea). A total of ca. 3 KB of sequence data of three mitochondrial and two nuclear genes were used to reconstruct the phylogeny of 62 specimens of 21 species of Hydrochus, including all western Mediterranean species but one. We estimated the times of divergence using Bayesian methods and an evolutionary rate of 0.0115 substitutions/site/MY, and used an ultrametric calibrated tree to construct a Lineage Through Time (LTT) plot to test alternative models of diversification. A well resolved, well supported phylogeny showed that all western Mediterranean Hydrochus formed a clade, sister to a group including species with a central and eastern European distribution. The origin of the western Mediterranean clade was estimated to be at ca. 13MY, and the speciation events took place between this time and the end of the Messinian, at about 5.3MY. The LTT plot best fitted a model with a shift in the rate of diversification at ca. 8 MY, with a single speciation event (originating two Iberian endemics) subsequent to this period. We conclude that most of the western Mediterranean species of Hydrochidae, including the Ibero-Maghrebian endemics, are ancient elements likely to have remained in the same geographical area since their Miocene origin. Our results add to a growing body of evidence showing the importance of Mediterranean long-term, Tertiary refugia as both cradles and museums of diversity.Work was funded with projects CGL2004-00028 and CGL2007-61665 to IR.Peer reviewe

Filogeografía del grupo Agabus brunneus (Dytiscidae: Coleoptera): evaluando/resolviendo una especiación reciente

Trabajo presentado en el I Congreso Ibérico de Sistemática Animal (CISA2012), celebrado en Madrid del 17 al 19 de enero de 2012.El grupo de especies de Agabus brunneus (Dytiscidae: Coleoptera) está compuesto de tres especies que presentan unos rangos de distribución muy distintos. Dos de ellas tienen un rango reducido (Agabus ramblae Millán y Ribera, 2001 en el SE Ibérico y Marruecos y Agabus rufulus Fairmaire, 1859 en Córcega y Cerdeña) mientras que la tercera se distribuye en gran parte de Europa y Norte de África (Agabus brunneus (Fabricius, 1798)). La diversificación en este grupo de especies es muy reciente, de manera que los marcadores mitocondriales empleados (cox1 y rrnL) no presentan suficiente variación para resolver la filogeografía del grupo. Evaluamos en este trabajo la capacidad de otro marcador (proteína de función desconocida) desarrollada para otra familia de coleópteros (Leiodidae) que presenta una variabilidad comparable a la del gen cox1. La separación inicial de estas tres especies se realizó en base a caracteres morfológicos del edeago y la morfología externa. Presentamos también un análisis morfométrico de varios caracteres del individuo y del edeago para confirmar esta separación.Peer reviewe

Hydrochus farsicus Hidalgo-Galiana, Jäch & Ribera, 2010, new species

Hydrochus farsicus, new species Figs 1–2 Type locality. Sepidan, Province of Fars, Iran. Type material. Holotype (NMW): “ 2 - IRAN Fars, 13.8. 1998 / 6km W Sepidan / rd. Sepidan-Yasuj / brook (Cheshmeh Saran) / leg. Elmi & Fery (# 2098)” and holotype label. Aedeagus glued on the same card. Base of aedeagus slightly damaged. Paratypes (NMW): Two females with the same data as holotype, plus paratype labels. Diagnosis. The only reliable characters to identify this new species are those of the male genitalia (Fig. 2). Other putative morphological characters may be shared with still undescribed, closely related species and are thus not reliable for an unambiguous identification. Description. Habitus as in Fig. 1. Elytra and body appendages brown, except apex of maxillary palpi and base of mandibles darker; head black; pronotum brown with central area darker; surface with light bluish or greenish metallic reflections. Ventral side evenly dark brown, except for head black. Head with deep, coarse evenly distributed punctures, intermixed with smaller punctures with short whitish setae; four small tubercles between eyes. Pronotum elongate, subcylindrical, wider anteriorly; with seven depressions, three anterior, rounder and four posterior, more elongate; lateral posterior depressions smaller, reaching posterior margin of pronotum. Punctation and pubescence as on head. Elytra subparallel-sided, slightly wider posteriorly; with 10 longitudinal striae formed by deep, regularly aligned punctures. Humeral region of elytra prominent. Tibiae with a regular dense row of setae in upper apical part; femora with evenly distributed small setae. Ventral surface covered with short, thick and dense pubescence, surface strongly microrecticulate, cells small and with a shagreen-like aspect. Medial line of ventrites, medial area of metaventrite, and two lateral areas in the metaventrite glabrous or with less dense pubescence. Ventrites with a strong transverse medial ridge, almost forming a carina. Aedeagus as in Fig. 2, 0.98 mm long, 0.3 mm wide; robust, parameres and median lobe asymmetrical: apex of left paramere with an asymmetrical triangular expansion; apex of right paramere sinuated, not expanded. Apex of median lobe expanded, poorly sclerotized, with a small flagellum. Variation. Length 3.2–3.4 mm; maximum width 1.0– 1.3 mm. Without apparent secondary sexual dimorphism. Distribution. Only known from the type locality. Remarks. The morphology of the aedeagus of H. farsicus resembles that of some Iberian species (Hydrochus ibericus Valladares, Díaz & Delgado and H. angusi Valladares), although it may also be related to the group of H. elongatus (Schaller), with a more eastern distribution (Hidalgo-Galiana et al., in preparation). Mart et al. (2009) recorded H. ibericus from Turkey, but unfortunately they did not figure the aedeagus and did not give details of the material used for comparison. Etymology. Named after the Iranian province of Fars, from where this species was collected.Published as part of Hidalgo-Galiana, Amparo, Jäch, Manfred A. & Ribera, Ignacio, 2010, Hydrochus farsicus sp. n. from Iran and notes on other Palearctic species of the genus (Coleoptera: Hydrophiloidea: Hydrochidae), pp. 61-64 in Zootaxa 2344 on pages 61-63, DOI: 10.5281/zenodo.19334

Hydrochus farsicus sp.n. from Iran and notes on other Palearctic species of the genus (Coleoptera: Hydrophiloidea: Hydrochidae)

The family Hydrochidae (or subfamily Hydrochinae for some authors) includes one recognised genus (Hydrochus Leach) with more than 200 species and a worldwide distribution (Hansen, 1999; Short & Hebauer, 2006). The West Mediterranean is among the most diverse areas for the genus in the Palearctic Region, with 12 species known from Spain and Morocco, including several endemic species described recently (Hansen, 2004). On the contrary, in the East Mediterranean and the Middle East few species are known so far, although some undescribed species from Turkey are deposited in the Naturhistorisches Museum Wien (NMW). No species of Hydrochus has ever been recorded from Iran (Hansen, 2004). Other groups of aquatic Coleoptera (e.g. Dytiscidae, Nilsson, 2004 or Hydraenidae, Jäch, 2004) display a more balanced distribution of species, and include a high number of Turkish or Iranian endemics. The situation in Hydrochus may be due to lack of knowledge, as the undescribed specimens in the NMW and some recent works (Incekara et al., 2004; Mart et al., 2009) may suggest, but it may be that in Turkey and the Middle East the genus Hydrochus is generally less speciose than in the West Mediterranean. In this paper two species of Hydrochus are recorded from Iran, one of which is described as new. In addition, some taxonomic notes on other Palearctic species are provided

Hydrochus farsicus sp. n. from Iran and notes on other Palearctic species of the genus (Coleoptera: Hydrophiloidea: Hydrochidae)

Hidalgo-Galiana, Amparo, Jäch, Manfred A., Ribera, Ignacio (2010): Hydrochus farsicus sp. n. from Iran and notes on other Palearctic species of the genus (Coleoptera: Hydrophiloidea: Hydrochidae). Zootaxa 2344: 61-64, DOI: 10.5281/zenodo.19334

Hydrochus nodulifer Reitter 1897

Hydrochus nodulifer Reitter, 1897 Material studied. One male (Coll. Pütz, Eisenhüttenstadt, Germany): IRAN: Prov. Gilan, Siahkal County, Elburz Mts., S-Slope, Deylaman-Barresar road, sifted, 1688 m, 36 º 51 '07''N, 49 º 49 ' 67.3 ''E, 07.VI. 2008, leg. A. Pütz “IR08- 25 ”. Remarks. First record for Iran. This species was described from “Elisabethpol” [= Ganja (or Ganca), Azerbaijan] (Reitter, 1897). A lectotype was designated by Shatrovskij (1993), who also figured the aedeagus. Hydrochus nodulifer has also been recorded from Eastern Anatolia and the Black Sea Area of Turkey (Mart et al., 2009).Published as part of Hidalgo-Galiana, Amparo, Jäch, Manfred A. & Ribera, Ignacio, 2010, Hydrochus farsicus sp. n. from Iran and notes on other Palearctic species of the genus (Coleoptera: Hydrophiloidea: Hydrochidae), pp. 61-64 in Zootaxa 2344 on page 63, DOI: 10.5281/zenodo.19334