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Karyotypes of two endemic species of hare from Ethiopia, Lepus habessinicus and L. starcki (Lagomorpha, Leporidae). A comparison with L. europaeus
Mammalia
Abstract
Karyotypes of two endemic species of hare from Ethiopia, Lepus habessinicus and L. starcki were studied and compared to that of L. europaeus. L. starcki has a fragmented range in the high Ethiopian plateaus and is considered a relict form of L. europaeus. In contrast, L. habessinicus occurs at lower altitudes, and is an arid-country species, The species share a 2n=48 and a FNa=88 common to all representatives of the genus. No sign of karyotypic differentiation is evident from G-banding and Ag-NOR location, These data support the hypothesis of pronounced karyotypic conservativism in the genus Lepus.
... The karyology of Lepus europaeus was studied by Schröder et al. (12), Zima and Kral (13), and Azzoroli Puccetti et al. (2) from Europe. The karyotype of the genus is characterized by a constant diploid number of 2n = 48 and a fundamental autosomal number of NFa = 88, as well as G-and C-banding patterns. ...
... Ag-NORs occurred at the telomeres of the short arms of 3 pairs of medium and small subtelocentric chromosomes (nos. 13, 16, and 20) in Lepus starckii examined from Ethiopia (2). NOR distribution in our specimens differed from that reported by Azzoroli Puccetti et al. (2). ...
... 13, 16, and 20) in Lepus starckii examined from Ethiopia (2). NOR distribution in our specimens differed from that reported by Azzoroli Puccetti et al. (2). Miller et al. (22) and Croce et al. (23) demonstrated that only functional NORs on chromosomes that were active in the preceding interphase could be detected by silver staining. ...
Conventional and GTC, CTC, and AgNO3 banded karyotypes of brown hares (Lepus europaeus Pallas, 1778) from Turkey are described for the first time. All specimens possessed a diploid number of 2n = 48 chromosomes and a fundamental autosomal number of NFa = 88. The chromosome set consisted of 8 metacentric and submetacentric pairs and 15 subtelocentric and acrocentric pairs decreasing in size from large to small. The X chromosome was a large submetacentric while the Y was a small acrocentric. In contrast with the other specimens, the Kilis specimen possessed a duplication in the long arm of one of the subtelocentric chromosomes. The G-banding pattern of the chromosomes was similar to that given for the genus. Variation was found in the C-banded karyotype and the distribution of NORs.
... The karyology of Lepus europaeus was studied by Schröder et al. (12), Zima and Kral (13), and Azzoroli Puccetti et al. (2) from Europe. The karyotype of the genus is characterized by a constant diploid number of 2n = 48 and a fundamental autosomal number of NFa = 88, as well as G-and C-banding patterns. ...
... Ag-NORs occurred at the telomeres of the short arms of 3 pairs of medium and small subtelocentric chromosomes (nos. 13, 16, and 20) in Lepus starckii examined from Ethiopia (2). NOR distribution in our specimens differed from that reported by Azzoroli Puccetti et al. (2). ...
... 13, 16, and 20) in Lepus starckii examined from Ethiopia (2). NOR distribution in our specimens differed from that reported by Azzoroli Puccetti et al. (2). Miller et al. (22) and Croce et al. (23) demonstrated that only functional NORs on chromosomes that were active in the preceding interphase could be detected by silver staining. ...
... The karyology of Lepus europaeus was studied by Schröder et al. (12), Zima and Kral (13), and Azzoroli Puccetti et al. (2) from Europe. The karyotype of the genus is characterized by a constant diploid number of 2n = 48 and a fundamental autosomal number of NFa = 88, as well as G-and C-banding patterns. ...
... Ag-NORs occurred at the telomeres of the short arms of 3 pairs of medium and small subtelocentric chromosomes (nos. 13, 16, and 20) in Lepus starckii examined from Ethiopia (2). NOR distribution in our specimens differed from that reported by Azzoroli Puccetti et al. (2). ...
... 13, 16, and 20) in Lepus starckii examined from Ethiopia (2). NOR distribution in our specimens differed from that reported by Azzoroli Puccetti et al. (2). Miller et al. (22) and Croce et al. (23) demonstrated that only functional NORs on chromosomes that were active in the preceding interphase could be detected by silver staining. ...
... The karyotype of the genus Lepus is conservative. Every member of this genus -including American samples of L. californicus (Worthington and Sutton, 1966) -has a diploid chromosome number (2n) of 48 and a fundamental number (FN) of 88 (Azzaroli Puccetti et al., 1996;Best, 1996;Robinson et al., 1983;Stock, 1976;Uribe-Alcocer et al., 1989). The only known exception is L. callotis with a FN = 90 (González and Cervantes, 1996). ...
... In addition, data from differentially stained karyotypes of several species of Lepus have shown that there is no evidence of non-Robertsonian chromosomal rearrangements in the species examined (Azzaroli Puccetti et al., 1996;Robinson et al. 1983). Chromosomal variation, therefore, is not a widespread phenomenon among jackrabbits. ...
... As expected, the Mexican populations of L. californicus and L. insularis both have the same diploid number present in other species of the genus Lepus. However, compared to previous findings on the FN of jackrabbits world wide (Azzaroli Puccetti et al., 1996;Best, 1996;González and Cervantes, 1996;Robinson et al., 1983;Uribe-Alcocer et al., 1989), both species of jackrabbits have fewer autosomal arms. American populations of L. californicus have an FN = 88 (Best, 1996;Robinson et al., 1983;Worthington and Sutton, 1966), whereas the Mexican specimens examined have an FN = 82. ...
We evaluated and compared the chromosomes of two species of Mexican jackrabbits. The 2n and FN of L. insularis were 48 and 80, respectively, whereas those of L. californicus were 48 and 82. The autosome morphology of L. insularis is four pairs of metacentric chromosomes, four pairs of submetacentric chromosomes, nine pairs of subtelocentric chromosomes and six pairs of telocentric chromosomes. In contrast, L. californicus had seven pairs of metacentric chromosomes, four pairs of submetacentric chromosomes, seven pairs of subtelocentric chromosomes, and five pairs of telocentric chromosomes. The X chromosome of L. insularis was medium-sized and submetacentric; the Y chromosome was small and telocentric, whereas both sex chromosomes of L. californicus
... Already Halanych et al. [130] noticed that Lepus species that are known to hybridize in the wild, such as L. europaeus and L. timidus, may nevertheless show marked mtDNA divergence, indicative of "good species". He hypothesized that geographic, ecological, or behavioural isolation mechanisms may be driving speciation in the genus Lepus rather than genetic incompatibility, also in view of the very little chromosomal variation within the genus (e.g., Robinson et al. [131,132], Azzaroli-Puccetti et al. [133]). Later studies are not incongruent with this hypothesis (e.g., Alves et al. [8], Liu et al. [9], Wu et al. [27], Melo-Ferreira et al. [10,11], see also Thulin et al. [7], and Robinson and Matthee [127]). ...
For hares (Lepus spp., Leporidae, Lagomorpha, Mammalia) from Ethiopia no conclusive molecular phylogenetic data are available. To provide a first molecular phylogenetic model for the Abyssinian Hare (Lepus habessinicus), the Ethiopian Hare (L. fagani), and the Ethiopian Highland Hare (L. starcki) and their evolutionary relationships to hares from Africa, Eurasia, and North America, we phylogenetically analysed mitochondrial ATPase subunit 6 (ATP6; n = 153 / 416bp) and nuclear transferrin (TF; n = 155 / 434bp) sequences of phenotypically determined individuals. For the hares from Ethiopia, genotype composition at twelve microsatellite loci (n = 107) was used to explore both interspecific gene pool separation and levels of current hybridization, as has been observed in some other Lepus species. For phylogenetic analyses ATP6 and TF sequences of Lepus species from South and North Africa (L. capensis, L. saxatilis), the Anatolian peninsula and Europe (L. europaeus, L. timidus) were also produced and additional TF sequences of 18 Lepus species retrieved from GenBank were included as well. Median joining networks, neighbour joining, maximum likelihood analyses, as well as Bayesian inference resulted in similar models of evolution of the three species from Ethiopia for the ATP6 and TF sequences, respectively. The Ethiopian species are, however, not monophyletic, with signatures of contemporary uni- and bidirectional mitochondrial introgression and/ or shared ancestral polymorphism. Lepus habessinicus carries mtDNA distinct from South African L. capensis and North African L. capensis sensu lato; that finding is not in line with earlier suggestions of its conspecificity with L. capensis. Lepus starcki has mtDNA distinct from L. capensis and L. europaeus, which is not in line with earlier suggestions to include it either in L. capensis or L. europaeus. Lepus fagani shares mitochondrial haplotypes with the other two species from Ethiopia, despite its distinct phenotypic and microsatellite differences; moreover, it is not represented by a species-specific mitochondrial haplogroup, suggesting considerable mitochondrial capture by the other species from Ethiopia or species from other parts of Africa. Both mitochondrial and nuclear sequences indicate close phylogenetic relationships among all three Lepus species from Ethiopia, with L. fagani being surprisingly tightly connected to L. habessinicus. TF sequences suggest close evolutionary relationships between the three Ethiopian species and Cape hares from South and North Africa; they further suggest that hares from Ethiopia hold a position ancestral to many Eurasian and North American species.
... Hybridization between more distantly related species argues that isolation mechanisms (e.g., geographic, behavioral, or ecological) may be driving speciation within Lepus. In fact, some workers Azzaroli Puccetti et al., 1996) have indicated that the lack of chromosomal diversity within Lepus points to mechanisms of speciation that do not invoke the chromosomal models suggested for other mammals (Reig, 1989;Dannelid, 1991). ...
Jackrabbits and hares, members of the genusLepus,comprise over half of the species within the family Leporidae (Lagomorpha). Despite their ecological importance, potential economic impact, and worldwide distribution, the evolution of hares and jackrabbits has been poorly studied. We provide an initial phylogenetic framework for jackrabbits and hares so that explicit hypotheses about their evolution can be developed and tested. To this end, we have collected DNA sequence data from a 702-bp region of the mitochondrial cytochromebgene and reconstructed the evolutionary history (via parsimony, neighbor joining, and maximum likelihood) of 11 species ofLepus,focusing on North American taxa. Due to problems of saturation, induced by multiple substitutions, at synonymous coding positions between the ingroup taxa and the outgroups (OryctolagusandSylvilagus), both rooted and unrooted trees were examined. Variation in tree topologies generated by different reconstruction methods was observed in analyses including the outgroups, but not in the analyses of unrooted ingroup networks. Apparently, substitutional saturation hindered the analyses when outgroups were considered. The trees based on the cytochromebdata indicate that the taxonomic status of some species needs to be reassessed and that species ofLepuswithin North America do not form a monophyletic entity.
... In addition to the plethora of earlier morphological revisions (not discussed here), the interspecific relationships of Lepus have been examined using chromosome banding, mtDNA gene sequences and in three instances, mtDNA in conjunction with nuclear sequences. All species of Lepus that have been karyotyped have 2n = 48 (Robinson, Elder & Chapman, 1983b and references therein; Azzaroli Pucetti et al., 1996; González & Cervantes, 1996; Lorenzo, Cervantes & Vargas, 2003 ), and differ only slightly in the amounts of pericentromeric heterochromatin. Karyotypic stability in this species may be a reflection of life history patterns, the recent radiation of species within the major evolutionary clades, genome stability and the species' greater propensity for movement (and hence gene flow). ...
ABSTRACT We review current knowledge of the evolutionary relationships among species of Leporidae drawing on molecular, cytogenetic and morphological data. We highlight problems associated with retrieving phylogenetic information under conditions of a rapid radiation and the lack of phylogenetically informative cytogenetic and mitochondrial DNA characters. Most morphological features underpinning generic distinctions are subtle and prone to reversal and convergence and as a consequence, they generally provide little basis for assessing phylogenetic affinity. We report the results of a supermatrix analysis that combines published nucleotide sequence data, unique insertion/deletion events, morphological characters and presumed geographical centres of origin of each genus. This represents the most comprehensive intergeneric comparison of the Leporidae thus far undertaken. The monophyly of the 11 leporid genera is unambiguously supported. There is support for an Afroasian assemblage that comprises Poelagus, Pronolagus and Nesolagus, a primitive Lepus, with the problematic Bunolagus, Oryctolagus, Caprolagus and Pentalagus as derived species in a clade that also includes the closely related Brachylagus and Sylvilagus as sister taxa. There is no support for the Palaeolaginae, although Romerolagus is an ancient lineage within the extant Leporidae. We hold that of the polytypic genera Lepus remains the most problematic, and provide a working hypothesis that will hopefully encourage future research on the various hare species.
... Previous studies have suggested that Lepus experienced rapid radiation [67,68]. The lack of chromosomal structural changes supports such a model of relatively recent, and rapid, diversification in this clade [69,70]. Low levels of genetic diversification between species could result in relatively fertile F 1 hybrids providing a bridge for further hybridization and thus introgression. ...
Interspecific hybridization may lead to the introgression of genes and genomes across species barriers and contribute to a reticulate evolutionary pattern and thus taxonomic uncertainties. Since several previous studies have demonstrated that introgressive hybridization has occurred among some species within Lepus, therefore it is possible that introgressive hybridization events also occur among Chinese Lepus species and contribute to the current taxonomic confusion.
Data from four mtDNA genes, from 116 individuals, and one nuclear gene, from 119 individuals, provides the first evidence of frequent introgression events via historical and recent interspecific hybridizations among six Chinese Lepus species. Remarkably, the mtDNA of L. mandshuricus was completely replaced by mtDNA from L. timidus and L. sinensis. Analysis of the nuclear DNA sequence revealed a high proportion of heterozygous genotypes containing alleles from two divergent clades and that several haplotypes were shared among species, suggesting repeated and recent introgression. Furthermore, results from the present analyses suggest that Chinese hares belong to eight species.
This study provides a framework for understanding the patterns of speciation and the taxonomy of this clade. The existence of morphological intermediates and atypical mitochondrial gene genealogies resulting from frequent hybridization events likely contribute to the current taxonomic confusion of Chinese hares. The present study also demonstrated that nuclear gene sequence could offer a powerful complementary data set with mtDNA in tracing a complete evolutionary history of recently diverged species.
... Divergence leading to speciation in Lepus is well within the realm of time of the Bering Strait closing. Due to the lack of chromosomal diversity within Lepus (Azzaroli Puccetti et al., 1996;) and hybridization between more distantly related spe- cies, concluded that isolation mechanisms (geographic, behavioral or ecological) contributed to Lepus speciation. Yamada et al. (2002) concluded that speciation within Lepus occurred in the early Pliocene (4–5 MYA) when taking into account that the split within Lepus occurred 12–16 MYA. ...
In spite of several classification attempts among taxa of the genus Lepus, phylogenetic relationships still remain poorly understood. Here, we present molecular genetic evidence that may resolve some of the current incongruities in the phylogeny of the leporids. The complete mitochondrial cytb, 12S genes, and parts of ND4 and control region fragments were sequenced to examine phylogenetic relationships among Chinese hare taxa and other leporids throughout the World using maximum parsimony, maximum likelihood, and Bayesian phylogenetic reconstruction approaches. Using reconstructed phylogenies, we observed that the Chinese hare is not a single monophyletic group as originally thought. Instead, the data infers that the genus Lepus is monophyletic with three unique species groups: North American, Eurasian, and African. Ancestral area analysis indicated that ancestral Lepus arose in North America and then dispersed into Eurasia via the Bering Land Bridge eventually extending to Africa. Brooks Parsimony analysis showed that dispersal events followed by subsequent speciation have occurred in other geographic areas as well and resulted in the rapid radiation and speciation of Lepus. A Bayesian relaxed molecular clock approach based on the continuous autocorrelation of evolutionary rates along branches estimated the divergence time between the three major groups within Lepus. The genus appears to have arisen approximately 10.76 MYA (+/-0.86 MYA), with most speciation events occurring during the Pliocene epoch (5.65+/-1.15 MYA approximately 1.12 +/- 0.47 MYA).
Starck’s hare (Lepus starcki Petter, 1963) is one of the endemic mammals of Ethiopia and potentially a very important part of the ecosystem. In this study, the food and habitat selection of Starck’s hare was investigated. To estimate the coverage of vegetation in the study area, the line intercept’ method was used. Diet was identified by analyzing faecal pellets and direct observation. Vegetation coverage was high (65.21%) during the wet season and low (<30%) during the dry season. The vegetation consisted of 27 plant species of which 21 were herbs, four grasses and 2 were shrubs. Monocotyledons occurred in higher percentage frequency in the diet of Starck’s hare during both seasons. Among the grasses, Festuca spp. was the most available and important food source for Starck’s hare during both seasons. The highest number of starck’s hares was recorded from rocky grass land during the wet season and from wetland during the dry season. Lepus starcki is an important component in the diet of the Ethiopian wolf and as a result proper management measures should be taken to conserve the endangered species.
The genomic location of rDNA in the rabbit was determined by in situ hybridization with 125I-labeled ribosomal RNA (rRNA). The results demonstrate the presence of rRNA genes on chromosomes 13, 16, and 20, all of which have secondary constrictions, and on the telomere of the long arm of 21. The number of genes, as assessed by grain counts, was not equally distributed among the chromosomes. Chromosome 20 had the most copies and along with 13 and 16 carried significantly more genes than 21.
Electrophoretic patterns show a difference in the result of restriction enzyme treatment of DNA from that hare occurring in the S part of the Iberian Peninsula (Lepus capensis) compared with DNA from the other two species (L. europaeus, L. castroviejoi). Hares in W Europe should thus be classified as different species, L. europaeus and L. capensis. As there is no difference in their DNA patterns, L. castroviejoi is suggested to be conspecific with L. europaeus.-from Authors
Some 665 hares were collected, predominantly from N Spain. Body and skull measurements, dental and skull characteristics, and pelage color and pattern indicated 3 species were present. They have different reproductive cycles, parapatric distribution with no overlap, and show different ecological behavior in neighbouring areas. Karyotypes were similar but lymphocyte DNA content and protein electrophoresis analyses were significantly different. The species were determined to be L. europaeus (N and NE Spain); L. granatensis (NE, W, central E and S Spain, Majorca and Portugal); and a new species, L. castroviejoi Palacios, 1976 (Cantabrian Mts).-Author
The present work completes the systematic treatment of Ethiopian mammals, commenced in 1973, by considering a diverse assemblage of species which presents the mammalogist with two quite distinct problems. Most of the larger forms are relatively free from taxonomic complexities, at least at the specific level, but rapidly declining in numbers as a result of drought, widespread destruction of natural habitat and inadequately controlled hunting. It appears that conservable stocks of pure-bred African Wild ass, Equus africanus (Fitzinger, 1857), now exist only in the Danakil region of Ethiopia, where the population is estimated to number no more than 2–3,000 head, while the herds of E. grevyi Oustalet, 1882 have been severely depleted during the past decade, both in this country and in neighbouring Kenya. The African Elephant, Loxodonta africana (Blumenbach, 1797), now occupies only remnants of its former range in Ethiopia and the position of the small Somali-arid race, L. a. orleansi Lydekker, 1907, is particularly precarious. It is believed that just 60–130 representatives of this subspecies still manage to survive in the valleys to the south of Harar, where they currently receive less than adequate protection. The status of the Red Sea Dugong, Dugong dugon hemprichi (Ehrenberg, 1833), also gives cause for concern, since here too there is evidence of a population which may well be dwindling towards extinction. If there is to be any hope for the continued survival of such animals, vigorous and effective programmes of conservation are required as a matter of urgency, yet it is equally apparent that wildlife authorities in Ethiopia still lack the resources to meet this demand and remain heavily dependent upon financial and technical assistance from external agencies. In the absence of action on an appropriate scale, it seems almost inevitable that many other large mammals will shortly repeat the dismal history of the Black rhinoceros, Diceros bicomis (Linnaeus, 1758), which is now virtually extinct in Ethiopia, its numbers reduced to a level where conservation has ceased to be a realistic proposition.
In contrast, many of the smaller mammals, including hyracoids and leporids, remain comparatively abundant in the field but present taxonomic problems which are often impossible to resolve because of the paucity of museum specimens or distributional data. Nomenclature within the genus Lepus is particularly perplexing but the authors believe there is good evidence for the recognition of four species in Ethiopia, including L. starcki Petter, 1963, which is endemic at altitudes of 2140–4000 m on the central plateaux.
The work concludes with a list of the 26 species of Cetacea which might conceivably enter Ethiopian waters or be stranded on the Ethiopian shoreline, but there seem to be rather few published records of marine mammals from this country and it is apparent that the cetacean fauna of the entire Red Sea area is very imperfectly known.
The chromosome banding patterns of the domestic rabbit, Oryctolagus cuniculus, the brush rabbit, Sylvilagus bachmani, and the snowshoe hare, Lepus americanus, are nearly identical except for minor differences in the amount of constitutive heterochromatin present. The major mechanisms of chromosome evolution in leporid lagomorphs are centric fusion and addition of heterochromatin. The G- and C-banding patterns of the pika, Ochotona princeps, revealed little easily recognized structural homology with the leporid species. Several tentative banding pattern matches were found for segments of some chromosomes of Ochotona, indicating that tandem fusions may have been responsible for structural modification of the early lagomorph genome. Chromosome evolution in the lagomorphs and the use of chromosomal data in studies of mammalian systematics are discussed.Copyright © 1976 S. Karger AG, Basel
G-banding of metaphase chromosomes in cultured lymphocytes was used to compare the karyotypes of two strains of domestic rabbit, Oryctolagus cuniculus (NZW and Dutch rabbit) and two species of hare (Lepus europaeus and Lepus timidus).
The NZW and the Dutch rabbit had identical karyotypes with 44 chromosomes, as did Lepus europaeus and Lepus timidus with 48 chromosomes.
However, all individual rabbits and hares showed chromosomal rearrangements (e.g. deletions and duplications) in 30–50% of all lymphocytes studied. The significance of the findings are discussed.
Nucleolar organizer regions (NOR's) were demonstrated in metaphase chromosomes of the domestic rabbit. Oryctolagus cuniculus (L.) (New Zealand white strain) using silver staining. Sequential quinacrine banding and a modification of the Ag-AS silver precipitation technique with duplicate photography allowed identification of silver staining NOR's on the short arms of chromosomes 13, 16, and 20, as well as the telomeric region of the long arms of number 21 in some cells. Chromosomes 13, 16 and 20 all have subterminal to terminal centromeres, often showed satellites and secondary constrictions, and were sometimes involved in associations.
The G- and C-banded chromosomes of six species of hare (genus Lepus) are presented and compared. No variation in gross chromosome morphology or banding pattern was observed indicating that speciation in this widespread genus has not involved karyotypic change.
Chromosome banding patterns of Lepus saxatilis, 2n = 48, and Pronolagus rupestris, 2n = 42, are presented. Comparison of G-banded karyotypes allows the identification of similar elements in both species. The karyotype of P. rupestris differs from that of L. saxatilis by the presence of three fusions in the former. Comparative studies with the fusion products of Oryctolagus cuniculus indicate that fusion and not fission is the major factor in chromosomal evolution of these leporids. The chromosomal conservatism of the hares is compared to the karyotypic variability of the rabbits and possible causes are discussed.