*Centre de Investigação em Biodiversidade e Recursos Genéticos (CIBIO/UP), Campus Agrário de Vairão, Vairão, Portugal;
Departamento de Zoologia-Antropologia, Faculdade de Ciências, Universidade do Porto, Praça Gomes Teixeira, Porto, Portugal;
Laboratoire de Génétique des Poissons, INRA, Jouy-en-Josas, France;
Department of Biology, Washington University, St. Louis
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Abstract |
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Introduction |
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Presently, many allozyme and protein loci have been subject to DNA sequencing and offer the opportunity to understand the genealogy of classical nuclear markers. Such an understanding could be especially useful where large data sets have been generated previously for such markers, allowing the choice of a locus exhibiting significant differentiation among populations at large and small geographic scales. That is the case of the transferrin (TF) locus, which is polymorphic in many vertebrate species, including fish (Kirpichnikov 1981, pp. 162168
). The locus codes an iron-binding protein found in vertebrate blood serum and interstitial spaces (Loehr 1989
, pp. 241243). Among salmonids, the locus has frequently been used to differentiate populations (e.g., Payne 1974
; Krieg and Guyomard 1985
; Van Doornik, Milner, and Winans 1996
) and, more recently, has received attention in studies of molecular adaptation (Ford, Thornton, and Park 1999
; Ford 2000
, 2001
).
In this context, the brown trout (Salmo trutta L.) is an appropriate organism to study the utility of nuclear gene genealogies for evolutionary inferences. This species exhibits a strong genetic structuring and is considered a polytypic species with complex patterns of phenotypic diversity and life history variation, including anadromous, fluviatile, and lacustrine modes of life (Behnke 1972
). Over the last two decades, geographic patterns of genetic differentiation were often observed, using both allozymes (e.g., Ryman, Allendorf, and Ståhl 1979
; Guyomard 1989
; Giuffra, Guyomard, and Forneris 1996
; Bouza et al. 1999
) and mtDNA (e.g., Bernatchez, Guyomard, and Bonhomme 1992
; Giuffra, Bernatchez, and Guyomard 1994
; Bernatchez and Osinov 1995
; Apostolidis et al. 1997
; Antunes et al. 2001
). The sequencing of the mtDNA control region delineated five major evolutionary lineages (Danubian [DA], Adriatic [AD], marbled trout [MA] found in some Adriatic drainages, Mediterranean [ME], and Atlantic [AT]; Bernatchez, Guyomard, and Bonhomme 1992
; Bernatchez 2001
) showing a strong distribution according to major drainage basins (fig. 1
). The distribution of allozyme variants is mostly congruent with these lineages (e.g., García-Marín, Utter, and Pla 1999
).
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Material and Methods |
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Estimation and Testing of Recombination-Gene Conversion
Detection of recombination-gene conversion events was performed using the CT algorithm of Crandall and Templeton (1999)
with additions given in Templeton et al. (2000a)
. The algorithm starts with the estimation of a haplotype "tree" under the null hypothesis of no recombination or gene conversion. The quotation marks placed around the word tree are to emphasize that this tree may not be an accurate reflection of the evolutionary history if the null hypothesis is rejected. From the checked robustness of the different tree topologies in Templeton et al. (2000a)
, we chose the statistical parsimony (SP) method for the tree estimation. SP (Templeton, Crandall, and Sing 1992
; Crandall 1994
; Crandall and Templeton 1996
) favors parsimonious solutions that avoid placement of homoplasies on short branches that lie within the "limit of parsimony" (Templeton, Crandall, and Sing 1992
). Maximum-parsimony trees were generated using PAUP (version 4.0b2a; Swofford 1998
). Comparison of the adjusted character distances with the corresponding patristic distances allowed the elimination of that maximum-parsimony trees that violated the limits of parsimony. The generated trees were also compared with the correspondent networks estimated in TCS (version 1.13; Clement, Posada, and Crandall 2000
).
After the tree estimation, the null hypothesis of no recombination was tested by means of associations between the positions of apparent homoplasies in the tree and the order of physical positions in the DNA sequence. This association is used in the CT algorithm to identify putative recombinants, tracing pathways through the tree, and to match the homoplasies clustered on a branch with their occurrences elsewhere in the tree. The algorithm also allows the identification of crossover intervals and candidate parental types. To identify statistically significant recombinants, a runs test based on a hypergeometric distribution was used. A program in MATHEMATICA (Wolfram 1996
) was written to perform those tests (Templeton et al. 2000a
).
The CT hypergeometric test is based on the ideal expectation of two runs under recombination: -matched homoplasious sites from one parental type defining a run on one end of the physical sequence, followed by a run of ß sites (i.e., the mutations on the pathway interconnecting the matched homoplasies) from the other parental type on the other end of the sequence. Gene conversion is another genetic mechanism for placing a physical cluster of nucleotide states on a new haplotype background. It can place a small run of variable sites from one haplotype into the middle of a second one, thereby yielding three runs by physical location. It can also result in only two runs, but such cases are indistinguishable from recombination. After the recombination tests were performed, an additional runs test was carried out to detect gene conversion events that have resulted in three or more runs. To test gene conversion with more than two runs,
-apparent homoplasies on a branch are matched with another region of the tree with ß-other mutations lying on the pathway between the two tree regions (Crandall and Templeton 1999
). The
+ ß mutations are then ordered by physical position, and the number of runs, say
, of
and ß mutations in the physically ordered sequence is recorded. Under the null hypothesis of no recombination-gene conversion, the probability for the number of runs, according to Mood and Graybill (1963, pp. 409412)
, is given by:
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Because gene conversion is tested only after recombination (d = 2), equations (1)
are used to calculate the probability of = 2 under the null hypothesis, and then equations (1)
are divided by [1 - Prob(
= 2)] to obtain the conditional distribution of runs, given that d
3, the only condition under which this gene conversion test is used. For more details, see the work of Crandall and Templeton (1999)
and Templeton et al. (2000a)
.
Inferring the Cladistic Structure in the Presence of Recombination-Gene Conversion
In this study we have inferred the cladistic structure of the TF gene using primarily an alternative and novel method recently proposed by Templeton et al. (2000b)
for removing the effects of recombination and estimating the cladistic structure in a DNA region that has experienced recombination. This approach has a broader range of applicability than the method of subdividing a gene into smaller regions that show little or no internal recombination (Templeton et al. 2000b
). The analysis starts by removing all inferred recombination events from the SP tree estimated for the entire DNA region. This means that the recombinant haplotypes identified by the CT algorithm are removed from the SP tree because homoplasies do not represent actual mutational events. All haplotypes and branches that are derived from such recombinant haplotypes by subsequent events are also removed. The remaining portion of the SP tree after this removal, the peeled tree, ideally reflects the component of haplotype diversity that has not been affected by recombination during the coalescence of this DNA region (Templeton et al. 2000b
). However, additional cladistic structure could have arisen in haplotype lineages derived from recombinant haplotypes. This postrecombinational cladistic structure is estimated by those subsets of the SP tree that consist of branches and haplotypes derived from each of the original recombinants by subsequent mutational events.
Tests of Neutrality
We tested the fit to the neutral expectations of nonsynonymous and synonymous segregating sites within brown trout using a contingency table (G-test; Templeton 1996
). From the inferred cladistic structure (peeled tree and recombinant clades), two tree topological mutational categories were used: tip and interior branches. The topological contrast of tip versus interior for the most part corresponds to a contrast of young versus old, thus yielding heterogeneity when selection occurs (i.e., tips are new and unproven, whereas interiors are older and have left descendants and thus have proven evolutionary success). Further, six functional mutational categories were considered: silent and replacement substitutions in hypothesized positively selected sites (PSSs) in salmonids (Ford 2001
), silent and replacement substitutions flanking PSSs (±3 codons), and silent and replacement substitutions in other sites. Two-by-two contingency tables were then analyzed using Fisher's exact test (FET) in STATISTICA (StatSoft 1993
). An exact permutational test on the entire two-by-six matrix was performed using CHIPERM (version 1.0; Posada 1998
).
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Results |
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Noncontiguous fragments of 3,696 bp (including indels) representing 44% of the full length of the TF gene (as compared with the homologous gene in medaka fish [Oryzias latipes]; Mikawa, Hirono, and Aoki 1996
) were sequenced in 31 brown trout and two Atlantic salmon individuals (table 1
; fig. 2
), describing a total of
122 kb analyzed (GenBank accession numbers AF488833AF489096). The aligned sequence data revealed 173 variable sites (excluding intraspecific variable sites within the Atlantic salmon), 113 of which varied within the brown trout. Of those, 106 (including 13 indels) were used for haplotype reconstruction and then for phylogenetic inferences (table 2
). The nucleotide divergence was slightly less for codon sites (table 3
).
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The a.a. sequences inferred from the translation of exons revealed 356 sites representing 52% of the total length of the TF protein in salmonids (Lee et al. 1998
). The aligned sequence data for all individuals revealed 13 different sequences with 27 variable positions, 15 of them varying within brown trout (fig. 4
). With the exception of two sites, all brown trout a.a. polymorphisms were biallelic (positions 312 and 320 had three alleles). The relation between electromorphs and their corresponding partial a.a. sequences revealed that some electromorphs have identical partial sequences (TF*78 and *80 = TFaa78.80; TF*101 and *102 = TFaa102), whereas TF*100 exhibited two different sequences (TFaa100-1 and TFaa100-2). TF*80, shared by Atlantic salmon and brown trout, exhibited very distinct a.a. sequences. The a.a. divergence among brown trout varied between 1.4% and 1.6%. The nucleotide divergence among haplotypes varied between 0.1% and 1.1%. Overall, we detect a strong correlation between the nucleotide and a.a. sequence and the correspondent electromorph.
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Detection of Statistically Significant Recombination-Gene Conversion Events
Two recombination and five gene conversion events were significant at the 5% level and were identified by applying the algorithm of Crandall and Templeton (1999)
to the null hypothesis tree. Figure 6
shows the tail probability from the hypergeometric test of the null hypothesis of no recombination and gene conversion and the spanned variable sites involved in the crossover event. Most of the variable sites were nucleotide substitutions, but a few involved insertions or deletions. Physical locations of recombinant sites comprise three regions in the gene: (I), a portion of exon 2 and intron 3, and intron 2; (II), a portion of intron 5; and (III), a portion of intron 9, and exons 10, 13, and 14 (fig. 3
). Recombination-gene conversion events were identified in regions (I), (II), and (III) at the following frequencies: 1, 3, and 2, respectively.
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Discussion |
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On the other hand, we found cases where a.a. differences between electromorphs were not detected in the partial nucleotide sequences analyzed. The distinct electromorph TF*101 was not differentiated at the sequence level from TF*102 because both had identical a.a. sequences and shared nucleotide haplotypes in the portion of the gene sequenced. Electromorphs TF*78 and *80 also exhibited identical a.a. sequences; however, nucleotide sequences were different between electromorphs. In both cases, the detected electrophoretic variation presumably results from mutations in other coding regions of the gene.
TF Gene Genealogy
One traditional method for estimating the cladistic structure in a DNA region subject to recombination involves removing the impact of recombination by splitting the DNA region into subsegments with little or no recombination (e.g., Templeton and Sing 1993
). However, the method would be difficult to implement under uniform recombination unless recombination was either rare or concentrated into hot spots (or both). Here, we implemented the method of Templeton et al. (2000b)
and identified three distinct areas of recombination and no single hot spot.
In spite of the observed recombination-gene conversion events in the portion of the TF gene analyzed, substantial cladistic structure was discriminated. The peeled tree (fig. 7
) provides an estimate of the cladistic structure contained within the 3.7-kb region sequenced that has not been altered by any detected recombination or gene conversion events. This peeled tree contains the branches leading to the three major termini (T-1, T-2, and T-3) that were defined primarily by sites 5' to the recombinational region I (fig. 3
). Moreover, the fact that the branches among the three major termini resulted in part from rare genomic changes (RGCs; Rokas and Holland 2000
) implies that this evolutionary structure is quite old.
Substantial cladistic structure has also arisen after recombination-gene conversion events (fig. 6
). Interestingly, those events provide evidence for secondary intergradation between distinct subclades. Some of these occur currently in the same geographic region, such as the TF95 and TF100 (Atlantic drainage), and the TF102 and TF78.80 (Mediterranean drainage) subclades. Gene conversion between subclades TF-BCA x TF102 and TF-BCA x TF75 currently occupying distinct geographic areas (Black, Caspian, and Aral Sea, as opposed to Adriatic and Mediterranean drainages), could represent a signature of past intergradations between those subclades. Additional evidence for secondary contact and introgressive hybridization is represented by the R1 and R2 haplotypes in individual 7, from the upper Danube. These haplotypes are related to the TF100 subclade, but they evolved by gene conversion and recombination events with other subclades (fig. 6
). This result is consistent with previous studies, which showed that some unstocked populations from the Danubian drainages or other Black Sea basins exhibit mtDNA and allozyme alleles specific to Atlantic brown trout (Bernatchez, Guyomard, and Bonhomme 1992
; Bernatchez and Osinov 1995
). The most likely explanation for this pattern is intergradation of ancient Danubian and Atlantic populations after secondary contact in postglacial times, a pattern that was also corroborated by other studies (e.g., Largiadèr and Scholl 1995
; Weiss et al. 2001
).
Tests of Neutrality
Results from the two-by-two contingency tests do not provide evidence for directional selection. This is because the absence of silent substitutions on PSSs precludes the application of the two-by-two test just to these sites. However, results of the two-by-six matrix test reject the null hypothesis of neutrality, largely because of the PSS and the total absence of silent substitutions. When compared with other sites, this would imply strong directional selection on the PSS. Ford, Thornton, and Park (1999)
suggested that positive natural selection for new alleles has played an important role in the evolution of the TF protein in salmonids. The selected sites generally fall on the outside of the molecule, within and near areas that are bound by TF-binding proteins from human pathogenic bacteria, thus supporting the hypothesis that competition for iron could be a source of positive selection (Ford 2001
). Ford (2000)
showed that unlike patterns of variation within species, there was no evidence of greater differentiation among chinook salmon (O. tshawytscha) populations at nonsynonymous compared with synonymous sites. Nevertheless, we do find some evidence for directional selection at the intraspecific level in the patterns of TF coding variation within brown trout, and thereby differences in the coalescence patterns among TF lineages may be expected (Takahata 1990
; Stephan and Mitchell 1992
).
Phylogeographic Assemblages of the TF Gene
On the basis of inferences from the TF genealogy and the current spatial distribution of electromorphs, we hypothesize a framework for the evolution of the S. trutta species complex (fig. 8
). The most ancestral group of populations is characterized by the TF-BCA subclade (present in Black, Caspian, and Aral Sea drainages). This conclusion is further supported by the fossil records. The oldest fossils of the brown trout were found in the Caucasus and date from early Pleistocene, 2 MYA (discussed in Osinov and Bernatchez 1996
). The radiation of the species could have started around this period, or even earlier. Some heterogeneity was observed among this haplogroup, with haplotypes from the Sevan Lake trouts (Caspian drainage) differing by at least nine substitutions from the others. The brown trout from Sevan Lake was initially hypothesized to be a species (S. ischchan) derived from the primitive ancestor of all brown trout populations (Behnke 1986
); however, this view has been contested on the basis of allozyme and mtDNA analyses which suggest that differentiation of this population occurred recently, most probably in late glacial or postglacial times (Bernatchez and Osinov 1995
; Osinov and Bernatchez 1996
). The observed divergence in the TF gene supports a more ancient origin than postglacial times for this population.
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The TF75 postrecombinant clade was found in the marbled trout (S. trutta marmoratus), which is a phenotypically and ecologically distinct brown trout currently present in Italy, Slovenia, Croatia, and Albania (Adriatic drainages) and typically fixed for TF*75 (Giuffra, Guyomard, and Forneris 1996
; Berrebi et al. 2000
). Based on allozyme data, Giuffra, Guyomard, and Forneris (1996)
proposed two alternative hypotheses for the colonization of the Po basin, depending on the order of arrival of the two natural forms that currently occur there (marbled and Mediterranean trout). Further allozyme evidence (Berrebi et al. 2000
) suggests that it was the marbled trout that was the last to arrive in the Adriatic region, and our data corroborate this hypothesis. The high divergence of this postrecombinant clade and the unique TF electromorph exhibited suggest, however, that the marbled trout arrived very early in this region. The presence of mtDNA haplotypes from the MA lineage in three Greek populations from the southern Adriatic-Ionian Sea drainage (Apostolidis et al. 1997
) and the detected gene conversion with the haplogroup BCA suggest that the origin of the postrecombinant clade TF75 could have been to the south of its current occurrence (fig. 8B
). The other subclade from the major terminus T-2, TF95, corresponding to the TF*95 electromorph, exhibits a very distinct range distribution relative to the previous one. At present, TF*95 mainly exists in relic populations of headwater systems. The electromorph is observed, at low frequencies, in the upper Rhône (Mediterranean) and Po (Adriatic) in Switzerland (Largiadèr and Scholl 1995
; Largiadèr, Scholl, and Guyomard 1996
), and at middle to high frequencies in some southwestern Atlantic upper stream populations from Portugal and Spain (Antunes, Alexandrino, and Ferrand 1999
; this study). Antunes, Alexandrino, and Ferrand (1999)
reported this puzzling trend and suggested that if common ancestry existed between the TF*95 from these distinct geographic regions, it would indicate the ancestral admixture of distinct geographic groups. Our data show that this electromorph has a rather old ancestry, further corroborated by its occurrence mainly in headwater drainages. The phylogenetic relationship of TF*95 with TF*75, together with their current distribution, suggests that the *95 electromorph went through a long-distance dispersal from the Adriatic region to the southernmost Atlantic regions (fig. 8B
). Because the Adriatic and Mediterranean drainages were already colonized habitats, dispersal was not so successful. By contrast, the Atlantic drainages of the Iberian Peninsula have offered the opportunity to colonize new habitats and continue range expansion to the west.
The major terminus T-3 is characterized by a codon insertion at exon 2. This is a derived brown trout characteristic differing from other salmonid cDNAs (Kvingedal, Aleström, and Rørvik 1993
; Lee et al. 1995
, 1998
; Tange et al. 1997
; Ford, Thornton, and Park 1999
; Ford 2000
). The mutation represents the signature of recent successful brown trout dispersal across most of its current distribution range (fig. 8C
). The postrecombinant clade TF78.80 was observed among populations from the Black Sea through the Mediterranean, whereas TF100 was present among the majority of the Atlantic populations. Divergence between these subclades reflects a recombination event and a second major dispersal event from the Mediterranean to the Atlantic drainages. Routes of dispersal do not seem to have been used very frequently, but rather in particular windows of time when climate and geography allowed. TF*78 is fixed for the Italian carpione (S. trutta carpio), an endemic form of Garda Lake (Po basin). This taxon is considered to be of postglacial origin, formed by recent hybridization between marbled trout and Mediterranean trout (Giuffra, Bernatchez, and Guyomard 1994
; Giuffra, Guyomard, and Forneris 1996
). Our results also support the introgressive hybridization origin of this form because we found one Italian carpione exhibiting a sequence related to the marbled trout postrecombinant clade (R3). The similarity in TF sequences between the two individuals from Garda Lake (Adriatic Sea drainage) and one individual from the very remote Kodori River (Black Sea drainage) is puzzling and suggests recent gene flow between these two remote areas. In contrast, we detected some sequence divergence in related haplotypes, corresponding to electromorph TF*80, found in the vicinity of the Adriatic drainage. TF*80 is currently observed in a few Mediterranean French (including Corsica) and Spanish populations (Presa et al. 1994
; Berrebi 1995
; this study). The distribution, both of TF*78 and *80, suggests a low level of penetration in previous established populations of the Adriatic and Mediterranean drainages. In contrast, the widespread distribution of subclade TF100 (corresponding to the electromorph TF*100) throughout the Atlantic drainage suggests a rapid expansion. The Atlantic basin was the one most directly affected by Pleistocene glaciations in terms of habitat loss, with later expansions overriding the range of earlier ones (Hewitt 2000
). The northern part of the Atlantic region was covered with ice during the last glaciation, and thus many populations have existed only since postglacial times (i.e., during the last 10,00018,000 years); however, the presence of discrete refugia in the southwestern Atlantic regions would have allowed persistence of some populations (e.g. Sanz, García-Marín, and Pla 2000
; Weiss et al. 2000
; Antunes et al. 2001
; Bouza et al. 2001
). This would explain part of the complexity found in the southernmost Atlantic populations, with the maintenance of some relic populations carrying the subclade TF95, and some structure within the subclade TF100.
Additional complexity in the brown trout evolutionary history was then added by the intergradation of differentiated subclades and postrecombination clades, as detected by some of the recombination-gene conversion events. Previous studies based on allozymes and mtDNA data identified introgressive hybridization between different lineages in glacial or postglacial times (e.g., Bernatchez, Guyomard, and Bonhomme 1992
; Largiadèr and Scholl 1995
; Osinov and Bernatchez 1996
); however, secondary intergradation (excluding that caused by stocking) seems to have been relatively limited (e.g., Bernatchez and Osinov 1995
; Giuffra, Guyomard, and Forneris 1996
). Biological factors, in addition to physical isolation, have probably limited dispersal and introgressive hybridization as can be inferred by the existence of five mtDNA lineages that evolved in geographic isolation during the Pleistocene and have remained largely allopatric since then (Bernatchez 2001
; fig. 1
).
Levels of Congruence with mtDNA Variation
The TF genealogy was consistent with some of the phylogenetic lineages recognized with the mtDNA. The brown trout from the BCA region (comprising populations geographically corresponding to the DA mtDNA lineage) seems to be mainly characterized by the TF-BCA haplogroup. The marbled trout (MA mtDNA lineage) is also characterized by just one postrecombinant clade (TF75). However, brown trout from other geographic areas exhibited TF haplotypes from different subclades. This is the case of brown trout from the Mediterranean and Adriatic basins (ME and AD mtDNA lineage, respectively) exhibiting the TF102 and TF78.80 subclades. Populations from the Atlantic basin (AT mtDNA lineage) exhibited the TF95 and TF100 subclades. The phylogeographic scenario inferred from the TF genealogy seems to predate that of the mtDNA. Whereas the mtDNA alleles have had sufficient time to sort to reciprocal monophyly, the alleles at the TF locus have not. Because mtDNA is haploid and maternally transmitted, it is expected to have a fourfold lower Ne than autosomal nuclear loci (Birky, Fuerst, and Maruyama 1989
). Under neutral models, the genetic drift governs the process of lineage sorting, and smaller effective population sizes (Ne) lead, on an average, to higher rates of stochastic lineage extinction and fixation (Hoelzer 1997
). This could also be a reason for the low mtDNA haplotype diversity found in the ME and MA lineages (three and four distinct haplotypes, respectively, in 104 and 205 individuals analyzed; Bernatchez 2001
). In contrast, our results, focusing on a small number of individuals, show a considerable number of distinct TF haplotypes corresponding to the major electromorphs that characterize these population groups.
The phylogenetic relationships of the TF gene show that haplotypes from the BCA region were those, among brown trout, exhibiting the highest similarity with the outgroup (fig. 7
). Some of this homology results from RGCs, which are character states that arise rarely and are not subjected to extensive convergent or parallel evolution, contributing to a low degree of homoplasy (Rokas and Holland 2000
). At the mtDNA level, the ancestral divergence of the AT lineage from all others was suggested when considering the Atlantic salmon as the outgroup (Giuffra, Bernatchez, and Guyomard 1994
; further discussed in Bernatchez 2001
) (fig. 1 ). The distinctness of the AT group was determined by the identity at four nucleotide positions with S. salar that differed in all other S. trutta genotypes, based on pooled sequences (1.25 kb) of both the control region and coding genes (cytochrome b and ATPase subunit VI). Assuming that the AT clade split from the ME or a common ancestor after the Messinian crisis (Machordom et al. 2000
), Antunes et al. (2001)
used a control region fragment of 464 bp and observed two statistically parsimonious solutions for the connecting branch of the two lineages. This suggests that because of the higher mutation level of mtDNA, even more homoplasy could be expected when comparisons are made at the generic level. According to our data, the TF100 subclade corresponding to the TF*100 electromorph that currently characterizes the majority of Atlantic populations is the most divergent from the outgroup.
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Conclusions |
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Acknowledgements |
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Footnotes |
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Keywords: brown trout
gene conversion
nuclear genealogy
recombination
Salmo trutta
salmonids
transferrin
Address for correspondence and reprints: Agostinho Antunes, Laboratory of Genomic Diversity, National Cancer Institute, Frederick, Maryland 21702-1201. aantunes{at}ncifcrf.gov
, aantunes{at}hotmail.com
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