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Molecular characterisation of the endangered Salamandra salamandra almanzoris (Caudata, Salamandridae)
Abstract and Figures
Salamandra salamandra is a polymorphic species with seven endemic subspecies in the Iberian Peninsula. Assignment of populations to subspecies in many areas is controversial because of discrepancies between morphological or molecular datasets. One potential intermixing area includes the Sistema Central Mountains, inhabited by S. s. almanzoris, a subspecies with a restricted distribution. In order to delimit the distribution area of S. s. almanzoris, we obtained sequences of the cytochrome-b gene in 84 individuals representing 26 populations covering the potential range of this subspecies and scored variation at 33 nuclear loci in ten of these populations through allozyme electrophoresis. S. s. almanzoris is fragmented into three disjoint groups of populations in the Sierras of Gredos, Guadarrama and San Vicente. The observation of (i) discordance between mtDNA and allozymes; (ii) coexistence of divergent mtDNA haplotypes in two populations; and (iii) discordance between external morphology and mtDNA haplotypes in different populations suggests recent events of secondary contact between S. s. almanzoris and other lineages within S. salamandra in the lowlands of the Sistema Central. We discuss the implications of these findings for the management of S. s. almanzoris populations in central Spain.
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... Across the Iberian Central System (ICS), populations from two distinct subspecies, S. s. bejarae and S. s. almanzoris, occur in parapatry across multiple regions associated to elevation gradients (Martínez-Solano et al. 2005;Pereira et al. 2016). The high-elevation subspecies S. s. almanzoris shows a restricted distribution in three isolated mountain tops, while the subspecies S. s. bejarae inhabits the surrounding lower elevation habitats ( Fig. 1). ...
... A previous study on this system revealed that the two subspecies are highly divergent at the mtDNA level ( Fig. 1), whereas nuclear DNA shows low or no differentiation across parapatric boundaries and high divergence across allopatric boundaries (Pereira et al. 2016). The highly divergent mtDNA lineages are fixed within populations and have been used to delineate the two subspecies, although they co-occur in regions of secondary contact (Martínez-Solano et al. 2005). The strong mito-nuclear discordances may result from a scenario of vicariant evolution leading to the differentiation of both subspecies followed by nuclearmediated gene flow across contact zones, potentially following range expansions from western refugia along the ICS (Pereira et al. 2016). ...
... Importantly, to avoid potential biases arising from uncertainties related with the distribution of each subspecies, our analyses do not rely on a priori assumptions regarding their classification. Instead, we identify evolutionary lineages based on our nuclear data and assign them to subspecies based on diagnostic mitochondrial data (Martínez-Solano et al. 2005) only a posteriori, to aid interpretation of results (detailed below). ...
Landscape features shape patterns of gene flow among populations, ultimately determining where taxa lay along the continuum between panmixia to complete reproductive isolation. Gene flow can be restricted, leading to population differentiation in two non-exclusive ways: “physical isolation”, in which geographic distance in combination with the landscape features restricts movement of individuals promoting genetic drift, and “ecological isolation”, in which adaptive mechanisms constrain gene flow between different environments via divergent natural selection. In central Iberia, two fire salamander subspecies occur in parapatry across elevation gradients along the Iberian Central System mountains, while in the adjacent Montes de Toledo Region only one of them occurs. By integrating population and landscape genetic analyses, we show a ubiquitous role of physical isolation between and within mountain ranges, with unsuitable landscapes increasing differentiation between populations. However, across the Iberian Central System, we found strong support for a significant contribution of ecological isolation, with low genetic differentiation in environmentally homogeneous areas, but high differentiation across sharp transitions in precipitation seasonality. These patterns are consistent with a significant contribution of ecological isolation in restricting gene flow among subspecies. Overall, our results suggest that ecological divergence contributes to reduce genetic admixture, creating an opportunity for lineages to follow distinct evolutionary trajectories.
... The greatest intraspecific diversity is seen within S. salamandra, where 12 to 17 subspecies are currently recognised, primarily based on colour patterns, geographic distribution, and a few additional morphological characters (Sparreboom, 2014;Thiesmeier, 2004;Thorn and Raffaëlli, 2001;Velo-Antón and Buckley, 2015;Raffaëlli, 2020). Most of these are found in the Iberian Peninsula (e.g., García-París et al., 2003;Martínez-Solano et al., 2005;Velo-Antón et al., 2007). Subspecies are also distinguished within S. atra (four subspecies; see Bonato et al., 2018), S. algira (five subspecies; ...
... As such, recognising it as a separate species would result in S. salamandra being paraphyletic. Moreover, patterns of introgression between S. s. almanzoris and its geographically neighbouring linage, S. s. bejarae, were detected across independent altitudinal gradients (Martínez-Solano et al., 2005;Pereira et al.., 2016). ...
The salamander genus Salamandra is widespread across Europe, North Africa, and the Near East and is renowned for its conspicuous and polymorphic colouration and diversity of reproductive modes. The phylogenetic relationships within the genus, and especially among the highly polymorphic species S. salamandra, have been very challenging to elucidate, leaving its real evolutionary history and classification at species and subspecies levels a topic of debate and contention. However, the distribution of diversity and species delimitation within the genus are critically important for identifying evolutionarily significant units for conservation and management, especially in light of threats posed by the pathogenic chytrid fungus Batrachochytrium salamandrivorans that is causing massive declines of S. salamandra populations in central Europe. Here, we conducted a phylogenomic analysis from across the taxonomic and geographic breadth of the genus Salamandra in its entire range. Bayesian, maximum likelihood and network-based phylogenetic analyses of up to 4,905 ddRADseq-loci (294,300 nucleotides of sequence) supported the distinctiveness of all currently recognised species (Salamandra algira, S. atra, S. corsica, S. infraimmaculata, S. lanzai, and S. salamandra), and all five species for which we have multiple exemplars were confirmed as monophyletic. Within S. salamandra, two main clades can be distinguished: one clade with the Apenninic subspecies S. s. gigliolii nested within the Iberian S. s. bernardezi/fastuosa; the second clade comprising all other Iberian, Central and East European subspecies. Our analyses revealed that some of the currently recognized subspecies of S. salamandra are paraphyletic and may require taxonomic revision, with the Central- and Eastern-European subspecies all being poorly differentiated in the analysed genomic markers. Salamandra s. longirostris – sometimes considered a separate species – was nested within S. salamandra, consistent with its subspecies status. The relationships identified within and between Salamandra species provide valuable context for future systematic and biogeographic studies, and help elucidate critical evolutionary units for conservation and taxonomy.
... Once regarded as a single highly polytypic species, the fire salamander group is now recognized as four distinct species , with more than 10 sub-species within S. salamandra alone 19 . At the same time, conflicting patterns of variation between traits have been frequently observed, and their analysis has formed the basis for intriguing insights into processes of reticulate evolution, range-change dynamics, and life-history traits evolution [21][22][23] . Consequently, the fire salamander is emerging as a compelling system for studying the contribution of multiple processes to the formation of intraspecific patterns of biological diversity 20 . ...
... 4,[27][28][29][30] ), but the extent of discordance observed in the present study is conspicuous. The geographic displacement between mitochondrial and nuclear contact zones among the two main lineages, largely exceeds the extent of discordances previously noted among fire salamander lineages from different geographic regions [21][22][23] , and has no parallels among different taxa from peninsular Italy. Interestingly, both mtDNA and nuclear contact zones are located within well known suture zones (sensu 31 ), where interspecific and intraspecific hybrid zones and range edges have been previously reported for various taxa, including amphibians (e.g. ...
Discordance between mitochondrial and nuclear patterns of population genetic structure is providing key insights into the eco-evolutionary dynamics between and within species, and their assessment is highly relevant to biodiversity monitoring practices based on DNA barcoding approaches. Here, we investigate the population genetic structure of the fire salamander Salamandra salamandra in peninsular Italy. Both mitochondrial and nuclear markers clearly identified two main population groups. However, nuclear and mitochondrial zones of geographic transition between groups were located 600 km from one another. The overall pattern of genetic variation, together with morphological and fossil data, suggest that a rampant mitochondrial introgression triggered the observed mitonuclear discordance, following a post-glacial secondary contact between lineages. Moreover, at a shallower level of population structure, we observed evidence of asymmetric introgression of nuclear genes between two sub-groups in southern Italy. Our results clearly show the major role played by reticulate evolution in shaping the structure of Salamandra salamandra populations and, together with similar findings in other regions of the species’ range, contribute to identify the fire salamander as a particularly intriguing case to investigate the complexity of mechanisms triggering patterns of mitonuclear discordance in animals.
... 4,27-32 ), but the extent of discordance observed in the present study is conspicuous. The geographic displacement between mitochondrial and nuclear contact zones among the two main lineages, largely exceeds the extent of discordances previously noted among fire salamander lineages from different geographic regions [21][22][23] , and has no parallels among different taxa from peninsular Italy. Interestingly, both mtDNA and nuclear contact zones are located within well-known suture zones (sensu 33 ), where interspecific and intraspecific hybrid zones and range edges have been previously reported for various taxa, including amphibians (e.g. ...
... Of course, given the many organismal functions in which the mitochondrial genome is implicated [45][46][47][48] , and the unsuitability of our data in this respect, we refrain from even hypothesizing which adaptive advantage might have promoted a massive mtDNA introgression. In light of the frequently observed mito-nuclear discordances in S. salamandra, at various levels of population structure [21][22][23] , we see this issue as a major research question, amenable to future experimental efforts. ...
Discordance between mitochondrial and nuclear patterns of population genetic structure is providing key insights into the eco-evolutionary dynamics between and within species, and their assessment is highly relevant to biodiversity monitoring practices based on DNA barcoding approaches. Here, we investigate the population genetic structure of the fire salamander Salamandra salamandra in peninsular Italy. Both mitochondrial and nuclear markers clearly identified two main population groups. However, nuclear and mitochondrial zones of geographic transition between groups were located 600 km from one another. Recent population declines in central Italy partially erased the genetic imprints of past hybridization dynamics. However, the overall pattern of genetic variation, together with morphological and fossil data, suggest that a rampant mitochondrial introgression triggered the observed mitonuclear discordance, following a post-glacial secondary contact between lineages. Our results clearly show the major role played by reticulate evolution in shaping the structure of Salamandra salamandra populations and, together with similar findings in other regions of the species' range, contribute to identify the fire salamander as a particularly intriguing case to investigate the complexity of mechanisms triggering patterns of mitonuclear discordance in animals.
... Aside from a large body of literature for terrestrial animals, phylogenies have been recently used to learn more about the evolutionary origins of aquatic organisms on the Balearic Islands. As a result, most aquatic groups have been attributed to colonization from the Iberian Peninsula (L azaro et al., 2011;Mart ınez-Solano, Alcobendas, Buckley, & Garc ıa-Par ıs, 2005;Muñoz et al., 2008) or northern Africa (Incagnone, Marrone, Barone, Robba, & Naselli-Flores, 2015) as single mainland source pools, whereas only few show multiple sources of origin (e.g., the planarian genus Dugesia Girard, 1850;L azaro et al., 2009). These studies, nevertheless, have focused mainly on species inhabiting the largest island of Majorca, and therefore dispersal events between islands or different faunal origins within the archipelago are difficult to detect (but see Brown et al., 2008, or Bauz a-Ribot et al., 2011 examples of the same species occurring in Majorca and Minorca). ...
Until recently, the evolutionary origin of aquatic organisms in the Balearic archipelago (western Mediterranean) had been scarcely addressed. The freshwater gastropod genus Pseudamnicola Paulucci, 1878 (Hydrobiidae), consisting of $60 species in the Mediterranean area, is widely distributed across the major islands of Majorca and Minorca. From phylogenetic datasets of limited geographic coverage, a recent well-supported split has been inferred between the Minorca and Iberian Pseudamnicola species, but the phylogenetic position of the Majorca clade composed of three species remained uncertain. In this study, we extend published sequence data for the COI and 16S rRNA mitochondrial genes and the 28S rRNA nuclear gene in western Mediterranean populations of Pseudamnicola with homologous sequences from individuals of the non-surveyed region of Morocco to assess the origin of the Balearic species from a wider geographic perspective. Our maximum likelihood and Bayesian inference analyses recovered a strongly supported clade comprising the Majorcan species and four phylogenetic lineages in Morocco, two of which are new to science (described here as P. ramosae sp. nov. and P. ouarzazatensis sp. nov.). Dating the nodes using an external molecular clock rate, younger ages were estimated for the Majorcan species ($1 Mya) than for the Moroccan ones ($5 Mya), which were still younger than the formation of the Balearic Islands ($30 Mya). An independent well-supported clade grouped the Minorca and Iberian species diverging at $4 Mya. Thus, we found two independent evolutionary origins within the Balearic archipelago likely attributable to long-distance dispersal events from the African and Eurasian continents. http://zoobank.org:pub:24D17C1D-4A42-4722-9867-D8D84465F55A http://zoobank.org:act:85EC4DF1-9BFA-4B28-B3F2-C091212AFCF1 http://zoobank.org:act:C790EAC6-F22B-489A-93EB-CABF9EEAF282
... Aside from a large body of literature for terrestrial animals, phylogenies have been recently used to learn more about the evolutionary origins of aquatic organisms on the Balearic Islands. As a result, most aquatic groups have been attributed to colonization from the Iberian Peninsula (L azaro et al., 2011;Mart ınez-Solano, Alcobendas, Buckley, & Garc ıa-Par ıs, 2005;Muñoz et al., 2008) or northern Africa (Incagnone, Marrone, Barone, Robba, & Naselli-Flores, 2015) as single mainland source pools, whereas only few show multiple sources of origin (e.g., the planarian genus Dugesia Girard, 1850;L azaro et al., 2009). These studies, nevertheless, have focused mainly on species inhabiting the largest island of Majorca, and therefore dispersal events between islands or different faunal origins within the archipelago are difficult to detect (but see Brown et al., 2008, or Bauz a-Ribot et al., 2011 examples of the same species occurring in Majorca and Minorca). ...
Until recently, the evolutionary origin of aquatic organisms in the Balearic archipelago (western Mediterranean) had been scarcely addressed. The freshwater gastropod genus Pseudamnicola Paulucci, 1878 (Hydrobiidae), consisting of ∼60 species in the Mediterranean area, is widely distributed across the major islands of Majorca and Minorca. From phylogenetic datasets of limited geographic coverage, a recent well-supported split has been inferred between the Minorca and Iberian Pseudamnicola species, but the phylogenetic position of the Majorca clade composed of three species remained uncertain. In this study, we extend published sequence data for the COI and 16S rRNA mitochondrial genes and the 28S rRNA nuclear gene in western Mediterranean populations of Pseudamnicola with homologous sequences from individuals of the non-surveyed region of Morocco to assess the origin of the Balearic species from a wider geographic perspective. Our maximum likelihood and Bayesian inference analyses recovered a strongly supported clade comprising the Majorcan species and four phylogenetic lineages in Morocco, two of which are new to science (described here as P. ramosae sp. nov. and P. ouarzazatensis sp. nov.). Dating the nodes using an external molecular clock rate, younger ages were estimated for the Majorcan species (∼1 Mya) than for the Moroccan ones (∼5 Mya), which were still younger than the formation of the Balearic Islands (∼30 Mya). An independent well-supported clade grouped the Minorca and Iberian species diverging at ∼4 Mya. Thus, we found two independent evolutionary origins within the Balearic archipelago likely attributable to long-distance dispersal events from the African and Eurasian continents.
http://zoobank.org:pub:24D17C1D-4A42-4722-9867-D8D84465F55A
http://zoobank.org:act:85EC4DF1-9BFA-4B28-B3F2-C091212AFCF1
http://zoobank.org:act:C790EAC6-F22B-489A-93EB-CABF9EEAF282
... However, García-París et al. (2003) and Iraola and García-París (2004) suggest that almanzoris belongs to a main clade with S. s. morenica and S. s. crespoi, making it impossible to treat the former as a species without consequences for the status of the other taxa. Martínez-Solano et al. (2005) showed that almanzoris is more widespread than traditionally considered, being distributed over most of the mountains of the Spanish Sistema Central. They found that the genetic divergence in allozymes between almanzoris and bejarae is typical for intraspecific levels in amphibians and that allozymes, morphology and mtDNA provide contrasting results on the delimitation of those taxa, evidencing introgression in contact zones. ...
Research on the taxonomy of European amphibians and reptiles has increased noticeably over the last few decades, indicating the need for recognition of new species and the cancellation of others. This paper provides a critical review of recent changes and draws up a tentative species list.
... It is widely accepted that the fire salamander is a polytypic species (Griffiths, 1996;Steinfartz et al., 2000;García-París et al., 2003;Martínez-Solano et al., 2005;Reis et al., 2011). Intraspecific differentiation is the most pronounced in the Iberian Peninsula where the ten subspecies were recognized (Steinfartz et al., 2000;García-París et al., 2003;Köhler & Steinfartz, 2006;Reis et al., 2011). ...
Morphological characteristics of the fire salamander population (Salamandra salamandra, Salamandridae) from Šar planina mountain
... It is most common in dark and damp areas litter-covered forest on the slopes of hills. It is widely accepted that the fire salamander is a polytypic species (Griffiths, 1996; Veith, 1997; Steinfartz et al., 2000; García-París et al., 2003; Martínez-Solano et al., 2005; Reis et al., 2011). Intraspecific differentiation is the most pronounced in the Iberian Peninsula where the ten subspecies were recognized (Steinfartz et al., 2000; García-París et al., 2003; Köhler & Steinfartz, 2006; Reis et al., 2011). ...
Key words: fire salamander, morphology, gender differences, qualitative traits. SYNOPSIS In this paper we present the results of the analysis of morphological characteristics of fire salamander population from Šar planina Mountain (Serbia). Univariant and multivariant statistical analyses have been performed on the samples taken from eight localities. The basic parameters of descriptive statistics for 17 morphometric characters have been calculated, separately by sexes. The analysis of variance (ANOVA) showed that sexes significantly differed in four characters. Males had larger forelimb length, hindlimb length and forefoot length, while females were larger in head width. Also, percentages of states for three qualitative traits were presented. Symmetrical pattern type of dorsal blotches prevails. Ključne riječi: šareni daždevnjak, morfologija, razlike među polovima, kvalitativne osobine. SINPOSIS MORFOLOŠKE KARAKTERISTIKE POPULACIJE ŠARENOG DAŽDEVNJAKA (Salamandra salamandra, Salamandridae) SA ŠAR PLANINE U radu su prikazani rezultati analize morfoloških karakteristika populacije šarenog daždevnjaka sa Šar planine (Srbija). Na uzorcima sakupljenim sa osam lokaliteta, urađene su univarijantne i multivarijantne statističke analize. Za 17 morfometrijskih karaktera izračunati su osnovni parametri deskriptivne statistike, odvojeno po polovima. Analiza varijanse (ANOVA) je pokazala da se polovi statistički razlikuju u četiri karaktera. Mužjaci imaju duže prednje ekstremitete, zadnje ekstremitete i stopala prednjih nogu, dok ženke imaju širu glavu. Takođe je izračunat i procenat zastupljenosti stanja, tri kvalitativne osobine. Preovlađuje simetričan tip dorzalne šare.
The number of subgenera within the genus Salamandra Garsault, 1764, is reduced from six to three, Salamandra Garsault, 1764, Alpandra Dubois & Raffaëlli, 2009 and Oriandra Dubois & Raffaëlli, 2009, following recent molecular results. Subgenus Algiandra Dubois & Raffaëlli, 2009 is here synonymized with the subgenus Salamandra and subgenera Corsandra Dubois & Raffaëlli, 2009 and Mimandra Dubois & Raffaëlli, 2009 with the subgenus Alpandra. Consequently, four new supraspecies are created to reflect the divergence between clades, respectively requalified as algira, corsica, lanzai and atra. Two subspecies within the supraspecies salamandra (Linnaeus, 1758), Salamandra salamandra carpathica (Călinescu, 1931) and Salamandra salamandra hispanica (Wolterstorff, 1937) are resurrected. A list of the 30 valid recognized taxa among the genus is presented.
With a standard set of primers directed toward conserved regions, we have used the polymerase chain reaction to amplify homologous segments of mtDNA from more than 100 animal species, including mammals, birds, amphibians, fishes, and some invertebrates. Amplification and direct sequencing were possible using unpurified mtDNA from nanogram samples of fresh specimens and microgram amounts of tissues preserved for months in alcohol or decades in the dry state. The bird and fish sequences evolve with the same strong bias toward transitions that holds for mammals. However, because the light strand of birds is deficient in thymine, thymine to cytosine transitions are less common than in other taxa. Amino acid replacement in a segment of the cytochrome b gene is faster in mammals and birds than in fishes and the pattern of replacements fits the structural hypothesis for cytochrome b. The unexpectedly wide taxonomic utility of these primers offers opportunities for phylogenetic and population research.
We studied the diet of 133 specimens of Salamaruha sdamandra dmanzoris from two sites in the Sierra de Gredos (province of Avila, Spain). The diet is basically insectivorous, consisting mainly of Coleoptera, Diplera and Pormicidae.. The food habits of this montane population differ notably from those in other areas within the Iberian Peninsula and Europe. We discuss our results in relation to the pecyliar habitats which Solarnondra salarnandra d m o r i a occupies in Gredos, and the trophic availability of the arthropods in the environment.
Esta guía tiene como objetivo la identificación de las 31 especies de anfibios y sus larvas y 83 especies de reptiles, tanto nativas como introducidas, que se encuentran en la península ibérica, islas Baleares e islas Canarias. Contiene claves de identificación, dibujos detallados (204 de anfibios y 302 de reptiles) y fotografías (95 de anfibios y 162 de reptiles) que muestran los caracteres de identificación más útiles. Con textos breves se pone énfasis en aquellas características que mejor distinguen a unas especies de otras. Además, se recoge de forma resumida información sobre su tamaño, distribución, hábitat, fenología, reproducción y estado de conservación. Se incluyen 112 mapas actualizados de distribución, con cuadrículas - 10 × 10 km.
Salamandra salamandra is a highly polytypic species characterized in the Iberian Peninsula by major differences in reproductive strategies, coloration patterns and morphological features. The aim of this paper is to focus on some aspects of this large phenotypic variability, especially the origin of differences in body size observed among populations. Skeletochronological methods were used to assess age and rates of bone growth in individuals from 14 populations throughout the Iberian Peninsula. Significant variation in the growth curves as well as in the relative growth rates were found among the populations sampled. Two bone growth patterns are recognizable. The population from Ronda (southern Spain) exhibits a basically linear growth rate through the first eight or more years of life instead of just four years as in the other populations. Such a linear growth rate means that for a given age (older than four years) the individual body size of salamanders from Ronda is higher than in other populations. All of the other populations show nonlinear growth curves. Bone growth rate is influenced by different factors (internal versus external) depending on the populations. The phenotypic variability encountered among the populations of salamanders from the Iberian Peninsula is, at least in part, caused by environmental conditions that influence the duration of the activity period of the salamanders and consequently the annual increase of growth. Nevertheless, the populations from northern Spain, characterized by some degree of viviparity (Lindus) or predominantly viviparous (Oviedo), show a significantly lower bone growth rate per month (mBGR) than the other populations. This lower mBGR, in addition to environmental factors, is responsible for the small body size observed in these populations.
— We studied sequence variation in 16S rDNA in 204 individuals from 37 populations of the land snail Candidula unifasciata (Poiret 1801) across the core species range in France, Switzerland, and Germany. Phylogeographic, nested clade, and coalescence analyses were used to elucidate the species evolutionary history. The study revealed the presence of two major evolutionary lineages that evolved in separate refuges in southeast France as result of previous fragmentation during the Pleistocene. Applying a recent extension of the nested clade analysis (Templeton 2001), we inferred that range expansions along river valleys in independent corridors to the north led eventually to a secondary contact zone of the major clades around the Geneva Basin. There is evidence supporting the idea that the formation of the secondary contact zone and the colonization of Germany might be postglacial events. The phylogeographic history inferred for C. unifasciata differs from general biogeographic patterns of postglacial colonization previously identified for other taxa, and it might represent a common model for species with restricted dispersal.
