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All issues No 421 (2020) Knowl. Manag. Aquat. Ecosyst., 421 (2020) 21 Full HTML
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Issue
Knowl. Manag. Aquat. Ecosyst.
Number 421, 2020
Article Number 21
Number of page(s) 16
DOI https://doi.org/10.1051/kmae/2020013
Published online 28 May 2020

© B. Delling et al., Published by EDP Sciences 2020

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License CC-BY-ND (https://creativecommons.org/licenses/by-nd/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. If you remix, transform, or build upon the material, you may not distribute the modified material.

1 Introduction

The taxonomic status of Eurasian trouts, i.e., all Salmo spp. except Atlantic salmon, Salmo salar, is revised continuously. Among molecular oriented ichthyologists, this part of Salmo diversity is most often referred to as brown trout Salmo trutta or “brown trout complex”, whereas taxonomic oriented scientists, mainly focusing on morphology, continue to describe new species and recognize at least 50 distinct taxa (Delling and Doadrio, 2005; Sušnik et al., 2006, 2007; Kottelat and Freyhof, 2007; Delling, 2010; Turan et al., 2009, 2011, 2012, 2014a, 2014b, 2017, 2020; Doadrio et al., 2015; Froese and Pauly, 2019).

The extensive molecular studies of the genus started mainly with allozymes (Ferguson and Mason, 1981; Karakousis and Triantaphyllidis, 1990; García-Marín et al., 1999; Berrebi et al., 2000a; Berrebi, 2015), later on shifting focus towards DNA sequencing mainly of mitochondrial origin (Giuffra et al., 1994; Apostolidis et al., 1997; Aurelle and Berrebi, 2001; Snoj et al., 2011). These studies led to numerous publications describing genetic variation in the genus. One of the most important findings within the taxonomic context is probably the proposed five main mitochondrial DNA (mtDNA) lineages within the brown trout complex, Atlantic (AT), Mediterranean (ME), Adriatic (AD), marble (MA) and Danubian (DA) (Bernatchez et al., 1992; Bernatchez, 2001). These lineages are augmented by geographically more limited lineages such as the Duero (DU) lineage (Suarez et al., 2001) and the Dades trout (Snoj et al., 2011), both close to AT, and the Tigris (TI) lineage (Bardakçi et al., 2006) close to DA. A recent analysis of a larger portion of the mtDNA allowed for a division of the AT lineage into two sister clades: a North African lineage (NA, in Morocco, Algeria and Sicily) and a well-known European AT lineage (Tougard et al., 2018).

In several cases, morphological and molecular data are correlated, strengthening hypotheses on taxa delimitation (Sanz, 2018). However, they sometimes disagree: for example, Salmo marmoratus, considered as very distinct in morphology (Delling, 2002), is also characterized by the MA mtDNA and the LDH-C1*(120) allozyme allele. However, MA haplotypes are also found in low frequencies outside the taxon (Bernatchez et al., 1992; Snoj et al., 2009; Pustovrh et al., 2011; Tougard et al., 2018) and the 120-allele is rare in Zadlascica River (Slovenia) otherwise pure and isolated S. marmoratus population (Berrebi et al., 2000b). Another example of markers disagreement is illustrated by S. obtusirostris. This species, while fixed for a unique and specific mtDNA haplotype in the Neretva River (Snoj et al., 2002), is fixed for the AD mtDNA lineage in Jadro River population. Other frequent kinds of contradiction have been observed, especially in the Balkans with numerous taxa sharing similar AD haplotypes (Sušnik et al., 2004, 2006; Snoj et al., 2010). These kinds of discrepancy may be explained by ancient introgression (Sušnik et al., 2007). Another explanation is the Dobzhansky–Muller model which accounts for cytonuclear incompatibilities (Burton and Barreto, 2012).

Despite the high number of more or less distinguishable taxa within the genus Salmo, large portions of its populations are not easily referred with accuracy to any existing taxon (Splendiani et al., 2019). This is partly due to lack of morphological data, lack of studies including both kinds of data and the fact that several tentatively valid taxa are poorly described lacking clear diagnoses (Kottelat and Freyhof, 2007). Within the native distribution of Salmo, a large part of its diversity is found in basins of the Tyrrhenian islands, Corsica, Sardinia and Sicily (Berrebi et al., 2019), and especially in Corsica where numerous differentiated indigenous populations still survive. Trout from Corsica and Sardinia, together with several other Mediterranean trouts, are often referred to as Salmo macrostigma (Duméril 1858) − a species originally described from Algeria. The name macrostigma refers to the parr marks retained in adults (Duméril, 1858). This is a common feature in many Salmo spp. and may explain the broadened usage of this name, as applied to Corsican trout by Roule (1933) and to Sardinian trout at first by Boulenger (1901) also confirmed by Pomini (1941). Since that, Corsican trout have been characterized both for allozymes (Guyomard and Krieg, 1986; Berrebi, 1995), mtDNA (Bernatchez et al., 1992; Berrebi et al., 2019) and microsatellites (Berrebi et al., 2007, 2019), showing that they mainly belong to the AD lineage and possess the highly diagnostic allozyme allele LDH3*(040). Morphological data on Corsican trout is so far restricted to pyloric caeca counts (Olivari and Brun, 1988; Guyomard, 1989) and the description of variation in color pattern among populations (Lascaux et al., 2010). In the same way, the non-introgressed Sardinian populations were characterized by only the AD lineage and allele LDH-C1 100/100 (Sabatini et al., 2018). Some authors describe, for the Sardinian populations, different haplotypes with highly polymorphic characteristics accompanied by different phenotypes (Sabatini et al., 2011; Zaccara et al., 2015; Berrebi et al., 2019).

Regarding distinctiveness of S. macrostigma sensu stricto, Tougard et al. (2018) analyzed complete mtDNA sequences from one syntype and one topotypic specimen and concluded they belonged to the NA lineage. In the same study, samples from Corsica and Sardinia were associated to AD, ME, MA or AT lineages.

The present study is deliberately “cross-disciplinary”, the main focus being to describe and discuss the Salmo diversity irrespective of different views on classification and taxonomy. Consequently, the use of different names, e.g. S. marmoratus or S. lourosensis, only serve the purpose of pointing out a certain subset of trouts. Both molecular and morphological data are presented and discussed for indigenous Salmo sp. from Corsica and Sardinia, here called Tyrrhenian trout. Regarding comparison to Algerian S. macrostigma, morphological data obtained from museum specimens are also included and discussed in the light of recent molecular findings (Tougard et al., 2018).

2 Material and methods

2.1 Sampling

Contemporary specimens (N = 38) from one Sardinian and six Corsican localities were captured in the wild by electrofishing, anesthetized with clove essence to death, sampled for tissue (fin clip in 95% ethanol), fixed in formalin 5%, and later transferred to ethanol prior to morphological analyses. The geographic positions of sampling stations are given in Figure 1. Tyrrhenian Salmo is referred to with an abbreviation of the stream, e.g. CAM for Camboni River in text, certain graphs and tables (Tab. 1). As detailed in Figure 1, samples for genetic and morphological analyses are not exactly the same.

Comparative material includes different sets of Salmo spp. depending on analyses and the question of interest: distinction towards (i) Salmo macrostigma from Algeria, (ii) Atlantic basin Salmo trutta, (iii) Salmo sp. from Spain. Comparative material for morphometry is restricted to specimens within standard length (SL) − range (116–208 mm), i.e., within the SL-range of Tyrrhenian trout samples. A description of contemporary and comparative material is given in Table 1, obtained from several museum collections: CMK, Collection of Maurice Kottelat, Cornol, Switzerland; BMNH, British Museum of Natural History, London, UK; MHNG, Museum d'Histoire Naturelle, Geneva, Switzerland; MNCN, Museo Nacional de Ciencias Naturales, Madrid, Spain; MNHN, Museum National d'Histoire Naturelle, Paris, France; NMW, Naturhistorisches Museum, Wien, Austria; NRM, Swedish Museum of Natural History, Stockholm, Sweden; ZISP, Zoological Institute, Russian Academy of Sciences, St. Petersburg, Russia; ZMH, Zoologisches Museum für Hamburg, Germany. The sample from Spain, MNHN 1920 228-229, consists of two specimens only but is included in the study because their morphology resembles Tyrrhenian trout (see below). Comparative material in addition to that in Table 1 (Delling, unpublished) is included for a broader comparison of head length within Salmo. A complete list of studied material is provided as supplementary information (Table S1).

thumbnail Fig. 1

Geographic position of the new sampled populations in Corsica and Sardinia.
Table 1

Studied material of Salmo from Sardinia and Corsica and selected comparative material (Tabs. 3–6). Catalog numbers are given for the Tyrrhenian samples only.

2.2 Molecular methods

DNA was extracted from fin clips using the Chelex/proteinase K protocol described by Estoup et al. (1996). Three to six individuals have been considered by locality in the Tyrrhenian region, being or not the exact individuals included in morphological analyses. Partial mtDNA control region (CR) was amplified by PCR using the PST and FST primers (Cortey and García-Marín, 2002). Each 50 µl reaction included 0.4 μM of each primer (Eurofins MWG Operon), 0.2 mM of dNTP (2 mM each), 2 mM of MgCl2 (25 mM), 10 µl of 5x PCR buffer, 1 U of Taq polymerase (GoTaq® Promega) and about 50 ng of genomic DNA. The conditions for PCR were an initial denaturation (95 °C, 5 min) followed by 30 cycles of strand denaturation (94 °C, 1 min), primer annealing (52 °C, 1 min) and DNA extension (72 °C, 1 min), then followed by a final extension (72 °C, 5 min). All PCR amplifications were performed in Eppendorf Mastercycler thermocyclers. The amplified DNA fragments were run on a 0.8% agarose gel to verify the efficiency of amplification. The PCR products were purified and sequenced in both directions to confirm polymorphic sites by the Macrogen Company, Seoul, South Korea (https://dna.macrogen.com/) and the platform GenSeq of the Institut des Sciences de l'Evolution de Montpellier (Montpellier, France).

The sequences of CR were aligned together with reference haplotypes retrieved from GenBank, using MEGA v5.05 (Tamura et al., 2011). Haplotypes for the new sequences were generated with DnaSP v5.10.1b (Librado and Rozas, 2009). Haplotype relationships and distribution among populations were evaluated with a median-joining network (Bandelt et al., 1999) constructed with PopART (Leigh and Bryant, 2015). In order to assign a phylogenetic position to the seven contemporary samples (CAM, SPE, POZ, ESE, CAR, CHA and NIN), the network included published GenBank sequences of the lineages AT, ME, AD, MA, DA and NA, all belonging to the brown trout complex.

2.3 Morphology methods

Methodology follows Delling et al. (2000) and Delling (2002). The length of the uppermost gill raker on the lower limb of the first gill arch (right side) was measured in situ using a pair of dividers. All other measurements were taken on the left side of the specimen with a digital calliper and rounded to the nearest 0.1 mm (Fig. 2). One important morphometric character in the present study is head length (HL) measured from tip of the snout to posterior margin of the operculum. However, the measurement that quantifies the size of the head more accurately is the distance from the premaxilla to the posterior margin of the preoperculum (No. 24 in Fig. 2). Below, the abbreviation HLpp is applied for that measurement.

The number of (i) pored scales along the lateral line to the end of the caudal peduncle (left side), (ii) scales in an oblique row from the base of the adipose fin backwards down to the lateral line including lateral line scales (left side), (iii) gill rakers, including rudimentary elements, on lower and upper limbs of the first gill arch separately (right side), and (iv) branchiostegal rays on both sides, were counted under a binocular dissection microscope.

The number of abdominal vertebrae, caudal vertebrae, pterygiophores supporting anal and dorsal fins, caudal fin upper and lower procurrent rays, and interneurals were taken from radiographs (Fig. 3). Rudimentary vertebrae in the caudal skeleton in addition to the three upturned vertebrae were not included in the counts. In cases of fused centra, the number of neural arches or spines was counted. The last abdominal vertebra is herein defined as the last one having ribs (sometimes rudimentary or missing) and/or having the haemal spine much shorter than in the consecutive first caudal vertebra. The positions of the dorsal and anal fins were estimated in relation to the vertebral column. The most strongly developed anterior pterygiophore was used as a marker of dorsal and anal fin position, respectively. Dorsal and anal fin pterygiophores do not articulate with neural and haemal spines, respectively, and in uncertain cases the lower value was chosen. The dorsal and anal fin positions are treated as meristic characters in statistical analyses. A membranous triangular bone sometimes present, located above the neural spine of the first vertebrae (Fig. 3), was not included in interneural counts.

Principal component analyses (PCA) on log transformed measurements and square rooted counts were used as an ordination method (Bookstein et al., 1985). Some informative meristic characters are summarised in frequency tables. The inclusion of ‘soft’ measurements, e.g. body width and body depth in analyses, depends on the state of preservation of specimens. PCAs were performed using SYSTAT 13. Colour pattern descriptions are most often restricted to contrasting markings: size, density and distribution of spots; presence of black and white leading edges of dorsal and anal fins; any other markings such as dark bars were also considered. In preserved material, light spots are interpreted as red spots based on personal observations: after transfer to ethanol, red spots disappear transformed into pale spots. Spots described as ocellated refer to spots enclosed by a light ring.

thumbnail Fig. 2

Measurements taken on Salmo specimens; 1, upper jaw depth, as largest depth of the maxilla and supramaxilla; 2, snout length, from symphysis of premaxilla to osseous orbit margin; 3, orbital horizontal diameter, between osseous orbital margin; 4, head depth, just posterior to orbit; 5, orbital vertical diameter, between osseous orbital margin; 6, length of maxilla, from premaxilla end to posterior end of maxilla; 7, upper jaw length, from symphysis of premaxilla to posterior end of maxilla; 8, lower jaw length, from symphysis of dentary to retroarticular; 9, pectoral fin length, from base of first ray to tip of longest ray; 10, body depth, at level of origin of dorsal fin; 11, dorsal fin length, from base to tip of longest ray; 12, pelvic fin length, from base of first ray to tip of longest ray; 13, body depth, at level of origin of anal fin; 14, adipose fin length, from origin to tip; 15, anal fin length, from base of first ray to tip of longest ray; 16, caudal peduncle length, from end of anal fin to middle base of caudal fin; 17, least depth of caudal peduncle; 18, length of upper caudal fin lobe, from base to tip of longest ray; 19, length of middle caudal fin ray, from base to tip of shortest ray; 20, length of lower caudal fin lobe, from base to tip of longest ray; 21 standard length (SL), from upper jaw symphysis to middle base of caudal fin; 22, predorsal length from upper jaw symphysis to origin of dorsal fin; 23, head length, from upper jaw symphysis to posterior tip of operculum; 24, premaxilla to preoperculum length, from premaxilla end of maxilla to posterior margin of preoperculum (HLpp); 25, prepelvic length, from upper jaw symphysis to origin of pelvic fin; 26, preanal length, from upper jaw symphysis to origin of anal fin; 27, interorbital width, transverse at narrowest part of skull; 28, body width, transverse at widest part of body at level of dorsal fin origin, above abdominal cavity.
thumbnail Fig. 3

Radiograph of Salmo sp. POZ, NRM62572, 197.3 mm SL; Pozzi di Marmanu Corsica (same specimen as in Fig. 8E). Upper left; a thin membranous bone indicated with dashed white line. Upper right; the uncommon condition with three (i-iii) epurals in the caudal skeleton.

3 Results

3.1 Molecular results

Among the 38 contemporary specimens from Corsica and Sardinia, 34 CR sequences were obtained, corresponding to eight new haplotypes (Tab. 2). The alignment of CR sequences are 998 nucleotides long with 47 phylogenetically informative sites. These haplotypes are genetically very close (distant from each other by up to two mutations, Fig. 4) to 37 published GenBank haplotype sequences used as reference and illustrating the diversity on all the range of the S. trutta complex. A comprehensive network of these new and published haplotypes is presented in Figure 4. The sequences of the contemporary analyzed populations were all clustered into ME, AD and MA lineages, according to the reference sequences. AT, DA and NA lineages were represented only by GenBank sequences.

New haplotypes from Tyrrhenian trout were called ADcr2 to 6, MAcr1 and 2, and MEcr1 (Tab. 2). Three populations are characterized by one private haplotype each: NIN, (Corsica) with MEcr1; CAM (Sardinia) with ADcr2 and POZ (Corsica) with ADcr4. CAR (Corsica) is characterized by a majority of MA private haplotypes (MAcr1 and 2) and one AD haplotype (ADcr5), while CHA (Corsica) is characterized by two AD haplotypes (ADcr3 and ADcr6). SPE and ESE shared ADcr3 with CHA.

Table 2

Distribution of the haplotypes involved in this study.

thumbnail Fig. 4

Median-joining network of control region haplotypes of some trout samples (new Tyrrhenian haplotypes and AT, AD, DA, MA, ME and NA haplotypes from GenBank). Haplotypes are indicated by numbers as given in Table 2. Black circles are for nodes, and hatch marks are for mutation steps.

3.2 Morphology

Morphometric data are given in Table 3, and meristic data are summarized in Tables 4–6 including extensive comparative material (Tabs. 1 and S1). Selected results from ordination by means of PCA are given for analyses focusing on variation between Tyrrhenian trout as a whole towards Atlantic basin S. trutta (Fig. 5). Corresponding character loadings are given in Supplementary Tables S2 and S3. The distinction of Tyrrhenian trout towards S. macrostigma is illustrated with a biplot (Fig. 6) focusing on the major morphological trait of the Tyrrhenian trout, viz. the longer head (HLpp) and slightly shorter caudal peduncle. The two Spanish specimens are included in all analyses and graphs. For discussion related to the comparatively large head in Tyrrhenian trout, HLpp is also presented as box plots in comparison to an extended number of Salmo samples (Fig. 7).

Table 3

Morphometry of Salmo spp. Number of studied specimens (N) for certain measurements varies due to condition of preserved specimens.

Table 4

Frequency distribution of scale counts from base of adipose fin to lateral line and left side branchiostegal counts in Salmo spp.

Table 5

Frequency distribution of vertebral counts and caudal fin upper procurrent rays in Salmo spp.

Table 6

Frequency distribution of gill raker counts in Salmo spp.

thumbnail Fig. 5

Morphometric PC II plotted against meristic PC I for Salmo from Sardinia, Corsica and Spain in comparison to Atlantic basin S. trutta.
thumbnail Fig. 6

Premaxilla to preoperculum length plotted against caudal peduncle length for Salmo from Sardinia, Corsica and Spain in comparison to S. macrostigma. Linear regression lines with 95% confidence bands are shown for each group separately.
thumbnail Fig. 7

Box plot of premaxilla to preoperculum length as % of SL, totally 518 specimens 116-208 mm SL. Number of specimens is given for each sample separately. Samples in bold are detailed in Table 1. Additional samples given in capital letters (Delling, unpublished) refer to rivers or streams in the given regions (Table S1). Ezenam is a lake in Daghestan and labrax represents trout from Black Sea basin with an anadromous silvery and slender appearance. Turkey and Mediterranean are samples scattered in the regions. Boxes represent median value +/− 25% of the observations, and whiskers the inner fences. Asterisks are outside or far outside values.

3.2.1 Variation among Tyrrhenian trout samples

At first glance (Fig. 8A–G), the Tyrrhenian trout resembles Atlantic basin S. trutta, i.e. rather strong jaws, numerous red and black spots, black and white edges of fins, most prominent in CAM, CAR, CHJ and SPE. Black spots are sometimes irregularly distributed, more or less aggregated along the flanks of the body (SPE, NIN) in contrast to, e.g., CAM having its spots more evenly distributed (Fig. 8A). There are large variations in meristic characters between different populations and the range of variation sometimes exceeds that of the extensive comparative material (Tabs. 4–6). The NIN sample and the two Spanish specimens were not markedly different in multivariate statistics in comparison to the six remaining samples.

Four specimens (1 POZ, 3 ESE) were different in the number of epurals in the caudal skeleton, having three instead of two. All Salmo except S. salar have two, sometimes fused (anomaly) to one. Salmo salar is polymorphic but two is more common (see below).

thumbnail Fig. 8

External aspect of seven of the trouts, Salmo sp., analyzed in the present study. Pictures A-F taken after fixation in formalin prior to transfer to ethanol.

3.2.2 Distinction of Tyrrhenian trout samples towards North Atlantic basin S. trutta

The rather strong jaws and a colour pattern with prominent black and white leading edges on the fins are shared between several populations of Atlantic basin S. trutta and the Tyrrhenian trouts. Dark, more or less ocellated, spots on flanks of the body are also common in both. However, some Tyrrhenian trout have their spots aggregated (Figs. 8F, 8G and p. 415 in Kottelat and Freyhof, 2007). The sample from Spain also possesses this uncommon pattern and was therefore especially highlighted in the comparative material. Sparsely or densely distributed, dark spots on caudal fin are also common in Tyrrhenian trout (Figs. 8B and 8G, CAM and SPE, respectively). Spots on caudal fins are rarely found in Atlantic basin S. trutta. Multivariate statistics (Fig. 5) indicate distinction but not complete separation of Tyrrhenian trout from Atlantic S. trutta due to differences in vertebral counts and head size.

3.2.3 Distinction of Tyrrhenian trout samples towards S. macrostigma

The extensive variation in meristic characters in Tyrrhenian trout as a whole (Tabs. 4–6) covers the range of variation in S. macrostigma and limits the analyses to morphometric data. PCA (not shown) reveals that HLpp and caudal peduncle length are the two morphometric characters that distinguish them best (Fig. 6). The Tyrrhenian trout has longer head (HLpp) and slightly shorter caudal peduncle compared to S. macrostigma (Tab. 3).

4 Discussion

4.1 Genetic diversity: a strong differentiation pattern

According to results from previous (Tougard et al., 2018; Berrebi et al., 2019) and present studies, the Tyrrhenian trout is mainly characterized by an island specific mtDNA-radiation within the AD lineage, as well as, to a lesser degree, by other lineages (AT, ME and MA). The recently described NA lineage is also naturally present in Sicily. Thus, within a rather limited and nowadays isolated region in the south center of Salmo distribution, a comparatively high number of mtDNA lineages (four of the five recognizable major lineages) occur naturally. It is also striking that a majority of the haplotypes recovered in the present study were new (Tab. 2) despite more than two decades of CR sequencing in Salmo. The presence of the ME lineage in the NIN sample, also observed in Corsica by Tougard et al. (2018) and in other Tyrrhenian samples not included in the morphological analyses, is explained by ancient introgressions evidenced elsewhere using nuclear markers (Berrebi et al., 2007; Berrebi, 2015). It shows that possible secondary contacts must have occurred, according to the post-glacial invasion of Corsica hypothesis (Gauthier and Berrebi, 2007). Moreover, the presence of MA lineage in some isolated Corsican rivers including CAR and the range of distribution of the NA lineage (Morocco, Algeria, Sicily: Tougard et al., 2018; Berrebi et al., 2019) demonstrates the multiple unknown events of migrations, invasions and hybridizations which complicate the trout genetic pattern in the Tyrrhenian region. Finally, the presence of several northern AT haplotypes recorded in the Tyrrhenian trout (Tougard et al., 2018; Berrebi et al., 2019) is due to stocking with commercial AT hatchery strains.

Nuclear markers (microsatellites) have also shown that the Tyrrhenian trouts exhibit exceptionally differentiated genotypes, at a continental-like level, within the two small sampled islands, but especially in Corsica where numerous autochthonous isolated small populations still survive (Berrebi et al., 2019). This strong differentiation among neighboring rivers is typical of dry Mediterranean mountainous regions, never frozen by glaciation and providing way for migration (Apostolidis et al., 2008; Berrebi et al., 2019).

4.2 Morphological diversity in light of genetic diversity

Regarding the strong morphological diversification between studied populations of Tyrrhenian trout, one explanation may involve random effects. Berrebi et al. (2019) showed very low levels of genetic variation within populations in Corsican streams based on microsatellites, suggesting small population sizes and repeated bottleneck events.

Hypothetically, the frequent (c. 10%) occurrence of three epurals in Tyrrhenian trout compared to c. 0.1% in comparative material might be a result of genetic drift accelerated by bottlenecks. Three epurals in the caudal skeleton are typical for, e.g., most Pacific trouts and salmons (Oncorhynchus), graylings (Thymallus) and whitefishes (Coregonus) (Norden, 1961; Stearley and Smith, 1993) and appear to be the ancestral state also retained as a polymorphism in S. salar with 12 out of 40 studied specimens having three.

Delling and Doadrio (2005) also described a situation with a seemingly plesiomorphic condition in rostrodermethmodid bone in the lake endemic S. pallaryi from Lake Sidi Ali, Morocco, not recorded elsewhere in Salmo. The genetic characteristics of this extinct trout is unknown but it is likely that these kinds of reversals approaching morphological anomalies may occur under certain conditions involving random processes in temporarily small populations.

Comparing Tyrrhenian samples to other Salmo spp., it is tempting to search for a pattern connecting certain characters to certain mtDNA lineages. However, ancient introgression in certain populations without strong impacts on morphology seems rather to be the “rule” in many salmonids and other taxa (Martinez et al., 2009; Gratton et al., 2013; Lerceteau-Köhler et al., 2013; Berrebi et al., 2017). The CAR sample also possessing the MA mtDNA lineage shows no typical S. marmoratus characters, e.g. marbled color pattern, high vertebral counts or a hypethmoid bone embedded in the rostral cartilage. In contrast, more recent hybrids involving S. marmoratus show a variable but, overall, intermediate phenotype (Delling et al., 2000). Prominent black and white leading edges on fins in several Tyrrhenian populations are similar to Atlantic basin S. trutta and could tentatively be regarded as ancient traces of the AT lineage. This pattern is also present in some North African trout, e.g. S. akairos and S. macrostigma belonging to the NA lineage, close to the AT one (Tougard et al., 2018). However, neither NA nor AT lineages have so far been reported from Corsica and Sardinia, except AT lineages of hatchery origin.

Despite the complex pattern of migrations, hybridizations and genetic radiation in the Tyrrhenian trout history, also giving rise to rather morphologically distinct populations in Corsica and Sardinia (Figs. 8A–G), they all share a comparatively large head (Figs. 6 and 7). This contradictory pattern of morphological homogeneity for certain characters opposed to strong differentiation in others take probably account of the genetic data in the search for possible explanations. Turning focus to the overall large head in Tyrrhenian trout, it is noticeable that this character varies extensively within and between different kinds of trouts (Fig. 7). It should be noted that sample sizes vary considerably (Fig. 7) but several of them can be characterized as typically small-headed, e.g., S. salar, S. obtusirostris and S. lourosensis. Next after the Tyrrhenian trouts, the two North African lake trouts endemic from Morocco, S. akairos and S. pallaryi, together with S. marmoratus and S. dentex inhabiting Adriatic basin drainages, possess comparatively large heads. Thus, there is no obvious correlation between size of head and habitat and/or lifestyle, e.g., rapid streams vs. lakes, and it is fully possible that the large head is a result of a founder effect during ancient establishment on the islands. However, body proportions can be affected by, e.g., growth rate. Barlow (1961) refers to studies where it was shown that head length was smaller in faster growing rainbow trout, Oncorhynchus mykiss. Thus, the comparatively large head in Tyrrhenian trout can be a consequence of slow growth under harsh condition, or a consequence of earlier sexual maturity. However, Pankhurst and Montgomery (1994) showed, also for O. mykiss, that retarded growth results in larger eyes. The Tyrrhenian trout possesses on the average slightly smaller eyes compared to Atlantic S. trutta (Tab. 3) and consequently retarded growth seems not to be a likely explanation for the large head.

The two Spanish specimens, referred to as Salmo sp. MNHN 1920 228-229, possess a color pattern with irregularly distributed spots, also found in some Tyrrhenian trouts, and are comparatively large headed (Fig. 6). They provide an example of what a hypothetical ancestor could have looked like and, if the interpretation of locality information (Ebro basin) is correct, it makes sense as the basin is dominated by AD haplotypes (Cortey et al., 2004). Also, the haplotype ADcs13 found in Ebro is very close to the Tyrrhenian AD haplotypes (Fig. 4).

5 Conclusions

Data presented herein suggest that within the rather unresolved Salmo complex in the Mediterranean region, we may start to perceive a kind of large headed trout. However, more populations from the islands and surrounding mainland (France, Spain, and Italy) need to be studied to survey the distribution of this morphology. It would be a large step forward if this kind of trout could get an identity, i.e. a scientific name to balance a perhaps too broad or erroneous usage of names such as S. trutta and S. macrostigma in the Mediterranean region. This long-term work already began with several recent molecular papers (Sanz, 2018; Tougard et al., 2018; Berrebi et al., 2019) and the present study. The Tyrrhenian trout studied here are left without a taxonomic identity but it is clearly demonstrated, in line with molecular data (Tougard et al., 2018), that they show no particular affinity to S. macrostigma once described from Algeria.

Supplementary Material

Supplementary Table S1. Supplementary Table S2. Supplementary Table S3.

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Acknowledgements

We thank Douglas Jones at the Institute of Freshwater Research, Drottningholm, for improving the English. This work was realized with the support of LabEx CeMEB, an ANR “Investissements d'avenir” program (ANR-10-LABX-04-01).

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Cite this article as: Delling B, Sabatini A, Muracciole S, Tougard C, Berrebi P. 2020. Morphologic and genetic characterisation of Corsican and Sardinian trout with comments on Salmo taxonomy. Knowl. Manag. Aquat. Ecosyst., 421, 21.

All Tables

Table 1

Studied material of Salmo from Sardinia and Corsica and selected comparative material (Tabs. 3–6). Catalog numbers are given for the Tyrrhenian samples only.

In the text
Table 2

Distribution of the haplotypes involved in this study.

In the text
Table 3

Morphometry of Salmo spp. Number of studied specimens (N) for certain measurements varies due to condition of preserved specimens.

In the text
Table 4

Frequency distribution of scale counts from base of adipose fin to lateral line and left side branchiostegal counts in Salmo spp.

In the text
Table 5

Frequency distribution of vertebral counts and caudal fin upper procurrent rays in Salmo spp.

In the text
Table 6

Frequency distribution of gill raker counts in Salmo spp.

In the text

All Figures

thumbnail Fig. 1

Geographic position of the new sampled populations in Corsica and Sardinia.
In the text
thumbnail Fig. 2

Measurements taken on Salmo specimens; 1, upper jaw depth, as largest depth of the maxilla and supramaxilla; 2, snout length, from symphysis of premaxilla to osseous orbit margin; 3, orbital horizontal diameter, between osseous orbital margin; 4, head depth, just posterior to orbit; 5, orbital vertical diameter, between osseous orbital margin; 6, length of maxilla, from premaxilla end to posterior end of maxilla; 7, upper jaw length, from symphysis of premaxilla to posterior end of maxilla; 8, lower jaw length, from symphysis of dentary to retroarticular; 9, pectoral fin length, from base of first ray to tip of longest ray; 10, body depth, at level of origin of dorsal fin; 11, dorsal fin length, from base to tip of longest ray; 12, pelvic fin length, from base of first ray to tip of longest ray; 13, body depth, at level of origin of anal fin; 14, adipose fin length, from origin to tip; 15, anal fin length, from base of first ray to tip of longest ray; 16, caudal peduncle length, from end of anal fin to middle base of caudal fin; 17, least depth of caudal peduncle; 18, length of upper caudal fin lobe, from base to tip of longest ray; 19, length of middle caudal fin ray, from base to tip of shortest ray; 20, length of lower caudal fin lobe, from base to tip of longest ray; 21 standard length (SL), from upper jaw symphysis to middle base of caudal fin; 22, predorsal length from upper jaw symphysis to origin of dorsal fin; 23, head length, from upper jaw symphysis to posterior tip of operculum; 24, premaxilla to preoperculum length, from premaxilla end of maxilla to posterior margin of preoperculum (HLpp); 25, prepelvic length, from upper jaw symphysis to origin of pelvic fin; 26, preanal length, from upper jaw symphysis to origin of anal fin; 27, interorbital width, transverse at narrowest part of skull; 28, body width, transverse at widest part of body at level of dorsal fin origin, above abdominal cavity.
In the text
thumbnail Fig. 3

Radiograph of Salmo sp. POZ, NRM62572, 197.3 mm SL; Pozzi di Marmanu Corsica (same specimen as in Fig. 8E). Upper left; a thin membranous bone indicated with dashed white line. Upper right; the uncommon condition with three (i-iii) epurals in the caudal skeleton.
In the text
thumbnail Fig. 4

Median-joining network of control region haplotypes of some trout samples (new Tyrrhenian haplotypes and AT, AD, DA, MA, ME and NA haplotypes from GenBank). Haplotypes are indicated by numbers as given in Table 2. Black circles are for nodes, and hatch marks are for mutation steps.
In the text
thumbnail Fig. 5

Morphometric PC II plotted against meristic PC I for Salmo from Sardinia, Corsica and Spain in comparison to Atlantic basin S. trutta.
In the text
thumbnail Fig. 6

Premaxilla to preoperculum length plotted against caudal peduncle length for Salmo from Sardinia, Corsica and Spain in comparison to S. macrostigma. Linear regression lines with 95% confidence bands are shown for each group separately.
In the text
thumbnail Fig. 7

Box plot of premaxilla to preoperculum length as % of SL, totally 518 specimens 116-208 mm SL. Number of specimens is given for each sample separately. Samples in bold are detailed in Table 1. Additional samples given in capital letters (Delling, unpublished) refer to rivers or streams in the given regions (Table S1). Ezenam is a lake in Daghestan and labrax represents trout from Black Sea basin with an anadromous silvery and slender appearance. Turkey and Mediterranean are samples scattered in the regions. Boxes represent median value +/− 25% of the observations, and whiskers the inner fences. Asterisks are outside or far outside values.
In the text
thumbnail Fig. 8

External aspect of seven of the trouts, Salmo sp., analyzed in the present study. Pictures A-F taken after fixation in formalin prior to transfer to ethanol.
In the text

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