Abstract
In recent years several new sportive lemur species (genus Lepilemur) have been described. In contrast to other lemur taxa, the genus shows comparatively high chromosomal variability, which, in addition to molecular data, can be used to infer phylogenetic relationships within the genus. By comparing R-banding patterns and fluorescence in-situ hybridization data, we detected chromosomal rearrangements that occurred during speciation within the genus. The analysis of these data with cladistic methods resulted in a dichotomic phylogenetic tree comparable to that obtained from mitochondrial sequence data. However, a phase of reticulation can not be excluded from the evolution of Lepilemur. Although some incongruences were detected, both phylogenies show similar patterns concerning relationships of the basal and terminal splits. We therefore hypothesize that both, chromosome rearrangements and molecular mutations, alone or in combination, contributed to the speciation process in sportive lemurs.
Similar content being viewed by others
Abbreviations
- CCD:
-
charge-coupled device
- DAPI:
-
4′,6-diamidino-2-phenylindole
- FISH:
-
fluorescence in-situ hybridization
- FITC:
-
fluorescein isothiocyanate
- HSA:
-
Homo sapiens
- MP:
-
maximum parsimony
- LAN:
-
Lepilemur ankaranensis
- LDO:
-
Lepilemur dorsalis
- LED:
-
Lepilemur edwardsi
- LEPI:
-
ancestor of the genus Lepilemur
- LLE:
-
Lepilemur leucopus
- LMI:
-
Lepilemur microdon
- LMT:
-
Lepilemur mittermeieri
- LRU:
-
Lepilemur ruficaudatus
- LSE:
-
Lepilemur septentrionalis
- MMR:
-
Microcebus murinus
- PAUP:
-
phylogenetic analysis using parsimony
References
Andriaholinirina N, Rabarivola C, Hauwy M, Rumpler Y (2005) Cytogenetic study of Lepilemur microdon. Folia Primatol 76: 238–241.
Andriaholinirina N, Fausser JL, Roos C et al. (2006a) Molecular phylogeny and taxonomic revision of the sportive lemurs (Lepilemur, Primates). BMC Evol Biol 6: 17.
Andriaholinirina N, Rabarivola C, Zaramody A et al. (2006b) Cytogenetic and molecular characterization of the newly described sportive lemur Lepilemur jamesi (Louis et al., 2006). Primate Report 74: 25–33.
Arnold ML, Meyer A (2006) Natural hybridization in primates: one evolutionary mechanism. Zoology 109: 261–276.
Avise JC, Wollenberg K (1997) Phylogenetics and the origin of species. Proc Natl Acad Sci U S A 94: 7748–7755.
Britton-Davidian J, Catalan J, da Graça Ramalhinho M et al. (2005) Chromosomal phylogeny of Robertsonian races of the house mouse on the island of Madeira: testing between alternative mutational processes. Genet Res 86: 171–183.
Craul M, Zimmermann E, Rasoloharijaona S, Randrianambinina B, Radespiel U (2007) Unexpected species diversity of Malagasy primates (Lepilemur spp.) in the same biogeographical zone: a morphological and molecular approach with the description of two new species. BMC Evol Biol 7: 83.
DelPero M, Crovella S, Cervella P, Ardito G, Rumpler Y (1995) Phylogenetic relationships among Malagasy lemurs as revealed by mitochondrial DNA sequence analysis. Primates 36: 431–440.
Dobigny G, Ducroz JF, Robinson TJ, Volobouev V (2004) Cytogenetics and cladistics. Syst Biol 53: 470–484.
Dutrillaux B, Couturier J, Muleris M, Rumpler Y, Viegas-Pequignot E (1986) Relations chromosomiques entre sous-ordres et infra-ordres, et schéma évolutif général des Primates. Mammalia 50: 108–121.
Hill WCO (1953) Primates: Comparative Anatomy and Taxonomy, Vol. 1, Strepsirrhini. Edinburgh: Edinburgh University Press.
Ishak B, Warter S, Dutrillaux B, Rumpler Y (1988) Phylogenetic relation between Lepilemuridae and other Lemuriform families. Am J Primatol 15: 275–280.
Ishak B, Warter S, Dutrillaux B, Rumpler Y (1992) Chromosomal rearrangements and speciation of sportive lemurs (Lepilemur species). Folia Primatol 58: 121–130.
Kehrer-Sawatzki H, Cooper DN (2008) Molecular mechanisms of chromosomal rearrangement during primate evolution. Chromosome Res 16: 41–56.
Lei R, Engberg SE, Andriantompohavana R et al. (2008) Nocturnal lemur diversity at Masoala National Park. Special Publications, Museum of Texas Tech University 53: 1–41.
Louis EE Jr, Engberg S, Lei R et al. (2006) Molecular and morphological analyses of the sportive lemurs (Family Megaladapidae: Genus Lepilemur) reveals 11 previously unrecognized species. Special Publications, Museum of Texas Tech University 49: 1–47.
Martin RD (2000) Origins, diversity and relationships of lemurs. Int J Primatol 21: 1021–1049.
Nei M (1987) Molecular Evolutionary Genetics. New York: Columbia University Press.
Pastorini J, Forstner MR, Martin RD (2002) Phylogenetic relationships among Lemuridae (Primates): evidence from mtDNA. J Hum Evol 43: 463–478.
Petit G (1933) Le genre Lepidolemur et sa répartition géographique. C R Soc Biogéogr 10: 33–37.
Petter JJ, Petter-Rousseaux A (1960) Remarque sur la systématique du genre Lepilemur. Mammalia 24: 76–86.
Petter JJ, Albignac R, Rumpler Y (1977) Mammifères lémuriens (Primates prosimiens). In: Faune de Madagascar, Vol. 44. Paris: CNRS/ORSTOM, pp. 1–513.
Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitutions. Bioinformatics 14: 817–818.
Qumsiyeh MB, Hamilton MJ, Schlitter DA (1987) Problems in using Robertsonian rearrangements in determining monophyly: examples from the genera Tatera and Gerbillurus. Cytogenet Cell Genet 44: 198–208.
Rabarivola C, Zaramody A, Fausser JL et al. (2006) Cytogenetic and molecular characteristics of a new species of sportive lemur from Northern Madagascar. Lemur News 11: 45–49.
Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.
Roos C, Schmitz J, Zischler H (2004) Primate jumping genes elucidate strepsirrhine phylogeny. Proc Natl Acad Sci U S A 101: 10650–10654.
Rumpler Y (2004) Complementary approaches of cytogenetics and molecular biology to the taxonomy and study of speciation processes in lemurs. Evol Anthropol 13: 67–78.
Rumpler Y, Dutrillaux B (1990) Chromosomal evolution and speciation in primates. Revis Biol Celular 23: 1–112.
Rumpler Y, Albignac R (1978) Chromosome studies of the Lepilemur, an endemic Malagasy genus of lemurs: contribution of the cytogenetics to their taxonomy. J Hum Evol 7: 11–196.
Rumpler Y, Ishak B, Dutrillaux B et al. (1986). Chromosomal evolution in Malagasy lemurs: IX. Chromosomal banding studies of Lepilemur mustelinus, L. dorsalis, and L. edwardsi. Cytogenet Cell Genet 42(3): 164–168.
Rumpler Y, Ravaoarimanana B, Hauwy M, Warter S (2001) Cytogenetic arguments in favour of taxonomic revision of Lepilemur septentrionalis species. Folia Primatol 72: 308–315.
Stanyon R, Rocchi M, Capozzi O et al. (2008) Primate chromosome evolution: ancestral karyotypes, marker order and neocentromeres. Chromosome Res 16: 17–39.
Strimmer K, von Haeseler A (1996) Quartet puzzling: a maximum likelihood method for reconstructing tree topologies. Mol Biol Evol 13: 964–969.
Swofford D (2002) PAUP*4.0b10 Phylogenetic analysis using parsimony (*and other methods). Sunderland, MA: Sinauer Associates.
Tattersall I (2007) Madagascar’s Lemurs: cryptic diversity or taxonomic inflation? Evol Anthropol 16: 12–23.
Thalmann U (2007) Biodiversity, phylogeography, biogeography and conservation: lemurs as an example. Folia Primatol 78: 420–443.
Vezuli A, Rumpler Y (2000) Lemur chromosomal study with simultaneous R-banding and chromosome painting. Chromosoma 109: 214–218.
Volobouev VT, Aniskin VM, Lecompte E, Ducroz JF (2002) Patterns of karyotype evolution in complexes of sibling species within three genera of African murid rodents inferred from the comparison of cytogenetic and molecular data. Cytogenet Genome Res 96: 261–275.
Warter S, Hauwy M, Dutrillaux B, Rumpler Y (2005) Application of molecular cytogenetics for chromosomal evolution of the Lemuriformes (Prosimians). Cytogenet Genome Res “Primate Cytogenetics” 108: (1–3): 197–203.
Wilmé L, Goodman SM, Goodman SM, Ganzhorn JU (2006) Biogeographic evolution of Madagascar’s microendemic biota. Science 312: 1063–1065.
Wyner YM, Johnson SE, Stumpf RM, DeSalle R (2002) Genetic assessment of a White-Collared X Red-Fronted lemur hybrid zone at Andringitra, Madagascar. Am J Primatol 67: 51–66.
Yoder AD (1994) Relative position of the Cheirogaleidae in strepsirrhine phylogeny: a comparison of morphological and molecular methods and results. Am J Phys Anthropol 94: 25–46.
Zinner D, Roos C, Fausser JL, Groves CP, Rumpler Y (2007) Disputed taxonomy classification of sportive lemurs (Lepilemur) in NW Madagascar. Lemur News 12: 53–56.
Acknowledgements
We thank the Direction des Eaux et Forêts of Antananarivo and Mahajanga, the Association Nationale pour la Gestion des Aires Protégées of Antananarivo and Mahajanga for their permission to do the field work. We thank the Faculty of Sciences of Antananarivo and the Institut Pasteur of Antananarivo for their support. We thank M. Lavaux for their technical assistance and V. Volobouev for his fruitful help with cladistic phylogeny. Grants came from A.E.E.C.L. and ULP-EA34280.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Rumpler, Y., Warter, S., Hauwy, M. et al. Comparing chromosomal and mitochondrial phylogenies of sportive lemurs (Genus Lepilemur, Primates). Chromosome Res 16, 1143–1158 (2008). https://doi.org/10.1007/s10577-008-1265-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10577-008-1265-z