Multilocus coalescent analyses reveal the demographic history and speciation patterns of mouse lemur sister species

BMC Evolutionary Biology

Volumn 14, Issue 1, 2014, Pages

  Blair, Christopher ^a   Heckman, Kellie L ^b   Russell, Amy L ^c   Yoder, Anne D ^a  

^a DUKE UNIVERSITY   (United States)

^b YALE UNIVERSITY   (United States)

^c GRAND VALLEY STATE UNIVERSITY   (United States)

Author keywords

Coalescent methods; Historical demography; Lemur evolution; Microcebus; Modes of speciation; Multilocus; Peripatric speciation

Indexed keywords

ALLOPATRY; ANTHROPOGENIC EFFECT; BIOMARKER; COALESCENCE; COMMON ANCESTRY; DEMOGRAPHIC HISTORY; DIVERGENCE; EFFECTIVE POPULATION SIZE; GENE FLOW; GENETIC ANALYSIS; GENETIC VARIATION; HYPOTHESIS TESTING; KINSHIP; NICHE PARTITIONING; PLEISTOCENE; PRIMATE; RANGE EXPANSION; SPECIATION (BIOLOGY);

MADAGASCAR;

ANIMAL; ARTICLE; CHEIROGALEIDAE; CLASSIFICATION; DEMOGRAPHY; EVOLUTION; FOUNDER EFFECT; GENETIC VARIABILITY; GENETICS; MADAGASCAR; MULTILOCUS SEQUENCE TYPING; PHYLOGENY; SPECIES DIFFERENTIATION;

ANIMALS; BIOLOGICAL EVOLUTION; CHEIROGALEIDAE; DEMOGRAPHY; FOUNDER EFFECT; GENETIC SPECIATION; GENETIC VARIATION; MADAGASCAR; MULTILOCUS SEQUENCE TYPING; PHYLOGENY;

EID: 84899080155     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-14-57     Document Type: Article

References (81)

1. Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Hey J, Nielsen R, Genetics 2004 167 2 747 760 10.1534/genetics.103.024182 15238526
2. Isolation with migration models for more than two populations. Hey J, Mol Biol Evol 2010 27 4 905 920 10.1093/molbev/msp296 19955477
3. The divergence of chimpanzee species and subspecies as revealed in multipopulation isolation-with-migration analyses. Hey J, Mol Biol Evol 2010 27 4 921 933 10.1093/molbev/msp298 19955478
4. Perspective: gene divergence, population divergence, and the variance in coalescence time in phylogeographic studies. Edwards S, Beerli P, Evolution 2000 54 6 1839 1854 11209764
5. Estimating effective population size from samples of sequences: inefficiency of pairwise and segregating sites as compared to phylogenetic estimates. Felsenstein J, Genet Res 1992 59 02 139 147 10.1017/S0016672300030354 1628818
6. Estimating effective population size and mutation rate from sequence data using metropolis-hastings sampling. Kuhner MK, Yamato J, Felsenstein J, Genet 1995 140 4 1421 1430
7. Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Beerli P, Felsenstein J, Genet 1999 152 2 763 773
8. The relationship between coalescence times and population divergence times. Rosenberg NA, Feldman MW, Modern Developments in Theoretical Population Genetics Oxford: Oxford University Press, Slatkin M, Veuille M, 2002 130 164
9. Bayesian species delimitation using multilocus sequence data. Yang Z, Rannala B, Proc Natl Acad Sci 2010 107 20 9264 9269 10.1073/pnas.0913022107 20439743
10. Statistical phylogeography. Knowles LL, Maddison WP, Mol Ecol 2002 11 12 2623 2635 10.1046/j.1365-294X.2002.01637.x 12453245
11. Speciational history of Australian grass finches (Poephila) inferred from thirty gene trees. Jennings WB, Edwards SV, Evol 2005 59 9 2033 2047
12. Working at the interface of phylogenetics and population genetics: a biogeographical analysis of Triaenops spp.(Chiroptera: Hipposideridae). Russell A, Ranivo J, Palkovacs E, Goodman S, Yoder AD, Mol Ecol 2007 16 4 839 851 10.1111/j.1365-294X.2007.03192.x 17284215
13. Ecological speciation. Rundle HD, Nosil P, Ecol Lett 2005 8 3 336 352 10.1111/j.1461-0248.2004.00715.x
14. Genomic consequences of multiple speciation processes in a stick insect. Nosil P, Gompert Z, Farkas TE, Comeault AA, Feder JL, Buerkle CA, Parchman TL, Proc Biol Sci 2012 279 1749 5058 5065 10.1098/rspb.2012.0813 22696527
15. Divergent selection and heterogeneous genomic divergence. Nosil P, Funk DJ, Ortiz-Barrientos D, Mol Ecol 2009 18 3 375 402 10.1111/j.1365-294X.2008. 03946.x 19143936
16. Peripatric speciation drives diversification and distributional pattern of reef hermit crabs (Decapoda: Diogenidae: Calcinus). Malay MCMD, Paulay G, Evol 2010 64 3 634 662 10.1111/j.1558-5646.2009.00848.x
17. Evolution of coral reef fish Thalassoma spp.(Labridae). 1. Molecular phylogeny and biogeography. Bernardi G, Bucciarelli G, Costagliola D, Robertson DR, Heiser J, Mar Biol 2004 144 2 369 375 10.1007/s00227-003-1199-0
18. Gene trees in species trees. Maddison WP, Syst Biol 1997 46 3 523 536 10.1093/sysbio/46.3.523
19. DNA barcoding: promise and pitfalls. Moritz C, Cicero C, PLoS Biol 2004 2 1529 1531
20. Recent trends in molecular phylogenetic analysis: where to next? Blair C, Murphy RW, J Hered 2011 102 1 130 138 10.1093/jhered/esq092 20696667
21. Taxonomic revision of mouse lemurs (Microcebus) in the western portions of Madagascar. Rasoloarison RM, Goodman SM, Ganzhorn JU, Int J Primatol 2000 21 6 963 1019 10.1023/A:1005511129475
22. Two new species of mouse lemurs (Cheirogaleidae: Microcebus) from eastern Madagascar. Rasoloarison RM, Weisrock DW, Yoder AD, Rakotondravony D, Kappeler PM, Int J Primatol 2013 34 3 455 469 10.1007/s10764-013-9672-1
23. Morphology, behaviour and molecular evolution of giant mouse lemurs (Mirza spp.) Gray, 1870, with description of a new species. Kappeler P, Rasoloarison R, Razafimanantsoa L, Walter L, Roos C, Primate Report 2005 71 3
24. Revision of the mouse lemurs (Microcebus) of eastern Madagascar. Louis EE Jr, Coles MS, Andriantompohavana R, Sommer JA, Engberg SE, Zaonarivelo JR, Mayor MI, Brenneman RA, Int J Primatol 2006 27 2 347 389 10.1007/s10764-006- 9036-1
25. First indications of a highland specialist among mouse lemurs (Microcebus spp.) and evidence for a new mouse lemur species from eastern Madagascar. Radespiel U, Ratsimbazafy JH, Rasoloharijaona S, Raveloson H, Andriaholinirina N, Rakotondravony R, Randrianarison RM, Randrianambinina B, Primates 2012 53 2 157 170 10.1007/s10329-011-0290-2 22198090
26. Review lecture: Adaptive radiation and behaviour of the Malagasy lemurs. Martin RD, Phil Trans Roy Soc Lond B Biol Sci 1972 264 295 352 10.1098/rstb.1972.0013
27. Tattersall I, Primates of Madagascar New York: Columbia University Press 52 1982
28. Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. Pearson RG, Raxworthy CJ, Nakamura M, Townsend Peterson A, J Biogeogr 2007 34 1 102 117
29. Population genetic analysis of Myzopoda (Chiroptera: Myzopodidae) in Madagascar. Russell AL, Goodman SM, Fiorentino I, Yoder AD, J Mammal 2008 89 1 209 221 10.1644/07-MAMM-A-044.1
30. Biogeographic evolution of Madagascar's microendemic biota. Wilmé L, Goodman SM, Ganzhorn JU, Sci 2006 312 5776 1063 1065 10.1126/science.1122806
31. Testing species-level diversification hypotheses in Madagascar: the case of microendemic Brookesia leaf chameleons. Townsend TM, Vieites DR, Glaw F, Vences M, Syst Biol 2009 58 6 641 656 10.1093/sysbio/syp073 20525615
32. Madagascar as a model region of species diversification. Vences M, Wollenberg KC, Vieites DR, Lees DC, Trends Ecol Evol 2009 24 8 456 465 10.1016/j.tree.2009.03.011 19500874
33. Mittermeier RA, Tattersall L, Konstant WR, Meyers DM, Mast RB, Lemurs of Madagascar Washington D.C: Conservation International 1994 1994
34. Remarkable species diversity in Malagasy mouse lemurs (primates, Microcebus). Yoder AD, Rasoloarison RM, Goodman SM, Irwin JA, Atsalis S, Ravosa MJ, Ganzhorn JU, Proc Natl Acad Sci 2000 97 21 11325 11330 10.1073/pnas. 200121897 11005834
35. Mouse lemur phylogeography revises a model of ecogeographic constraint in Madagascar. Yoder AD, Heckman KL, Primate Biogeography New York: Springer 2006 255 268
36. The ever-increasing diversity in mouse lemurs: three new species in north and northwestern Madagascar. Olivieri G, Zimmermann E, Randrianambinina B, Rasoloharijaona S, Rakotondravony D, Guschanski K, Radespiel U, Mol Phylogenet Evol 2007 43 1 309 327 10.1016/j.ympev.2006.10.026 17197200
37. Sympatric mouse lemurs (Microcebus spp.) in western Madagascar. Schmid J, Kappeler P, Folia Primatol 1994 63 3 162 170 10.1159/000156812 7750864
38. Sympatric mouse lemurs in north-west Madagascar: a new rufous mouse lemur species (Microcebus ravelobensis). Zimmermann E, Cepok S, Rakotoarison N, Radespiel U, Folia Primatol 1998 69 2 106 114 10.1159/000021571 9583951
39. Molecular evidence of reproductive isolation in sympatric sibling species of mouse lemurs. Yoder AD, Burns MM, Génin F, Int J Primatol 2002 23 6 1335 1343 10.1023/A:1021187106641
40. Hybridization between mouse lemurs in an ecological transition zone in southern Madagascar. Gligor M, Ganzhorn J, Rakotondravony D, Ramilijaona O, Razafimahatratra E, Zischler H, Hapke A, Mol Ecol 2009 18 3 520 533 10.1111/j.1365-294X.2008.04040.x 19161471
41. Hybridization of mouse lemurs: different patterns under different ecological conditions. Hapke A, Gligor M, Rakotondranary SJ, Rosenkranz D, Zupke O, BMC Evol Biol 2011 11 1 297 10.1186/1471-2148-11-297 21989384
42. Origins, diversity and relationships of lemurs. Martin RD, Int J Primatol 2000 21 6 1021 1049 10.1023/A:1005563113546
43. Multiple nuclear loci reveal patterns of incomplete lineage sorting and complex species history within western mouse lemurs (Microcebus). Heckman KL, Mariani CL, Rasoloarison R, Yoder AD, Mol Phylogenet Evol 2007 43 2 353 367 10.1016/j.ympev.2007.03.005 17446091
44. Delimiting species without nuclear monophyly in Madagascar's mouse lemurs. Weisrock DW, Rasoloarison RM, Fiorentino I, Ralison JM, Goodman SM, Kappeler PM, Yoder AD, PLoS One 2010 5 3 9883 10.1371/journal.pone.0009883 20360988
45. Incongruence between genetic and morphological diversity in Microcebus griseorufus of Beza Mahafaly. Heckman KL, Rasoazanabary E, Machlin E, Godfrey LR, Yoder AD, BMC Evol Biol 2006 6 1 98 10.1186/1471-2148-6-98 17109740
46. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Bioinformatics 2012 28 12 1647 1649 10.1093/bioinformatics/bts199 22543367
47. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Katoh K, Misawa K, Kuma K, Miyata T, Nucleic Acids Res 2002 30 14 3059 3066 10.1093/nar/gkf436 12136088
48. RDP3: a flexible and fast computer program for analyzing recombination. Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P, Bioinformatics 2010 26 19 2462 2463 10.1093/bioinformatics/btq467 20798170
49. Possible emergence of new geminiviruses by frequent recombination. Padidam M, Sawyer S, Fauquet CM, Virol 1999 265 2 218 225 10.1006/viro.1999.0056
50. Analyzing the mosaic structure of genes. Smith JM, J Mol Evol 1992 34 2 126 129 1556748
51. RDP: detection of recombination amongst aligned sequences. Martin D, Rybicki E, Bioinformatics 2000 16 6 562 563 10.1093/bioinformatics/16.6.562 10980155
52. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Librado P, Rozas J, Bioinformatics 2009 25 11 1451 1452 10.1093/bioinformatics/ btp187 19346325
53. Development and application of a phylogenomic toolkit: resolving the evolutionary history of Madagascar's lemurs. Horvath JE, Weisrock DW, Embry SL, Fiorentino I, Balhoff JP, Kappeler P, Wray GA, Willard HF, Yoder AD, Genome Res 2008 18 3 489 499 10.1101/gr.7265208 18245770
54. Delimiting species without monophyletic gene trees. Knowles LL, Carstens BC, Syst Biol 2007 56 6 887 895 10.1080/10635150701701091 18027282
55. Bayesian inference of population size history from multiple loci. Heled J, Drummond A, BMC Evol Biol 2008 8 1 289 10.1186/1471-2148-8-289 18947398
56. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Drummond AJ, Suchard MA, Xie D, Rambaut A, Mol Biol Evol 2012 29 8 1969 1973 10.1093/molbev/mss075 22367748
57. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Guindon S, Gascuel O, Syst Biol 2003 52 5 696 704 10.1080/10635150390235520 14530136
58. jModelTest 2: more models, new heuristics and parallel computing. Darriba D, Taboada GL, Doallo R, Posada D, Nature Methods 2012 9 8 772
59. Divergence dates for Malagasy lemurs estimated from multiple gene loci: geological and evolutionary context. Yoder AD, Yang Z, Mol Ecol 2004 13 4 757 773 10.1046/j.1365-294X.2004.02106.x 15012754
60. Bayesian inference of species trees from multilocus data. Heled J, Drummond AJ, Mol Biol Evol 2010 27 3 570 580 10.1093/molbev/msp274 19906793
61. Relaxed phylogenetics and dating with confidence. Drummond AJ, Ho SY, Phillips MJ, Rambaut A, PLoS Biol 2006 4 5 88 10.1371/journal.pbio.0040088 16683862
62. Tracer v1. 4. Rambaut A, Drummond A, 2007 http://beast.bio.ed.ac.uk/ Tracer
63. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Stamatakis A, Bioinformatics 2006 22 21 2688 2690 10.1093/bioinformatics/btl446 16928733
64. A rapid bootstrap algorithm for the RAxML web servers. Stamatakis A, Hoover P, Rougemont J, Syst Biol 2008 57 5 758 771 10.1080/10635150802429642 18853362
65. On the estimation of ancestral population sizes of modern humans. Yang Z, Genet Res 1997 69 2 111 116 10.1017/S001667239700270X 10191720
66. Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Chen F-C, Li W-H, Am J Hum Genet 2001 68 2 444 456 10.1086/318206 11170892
67. Speciation in little: the role of range and body size in the diversification of Malagasy mantellid frogs. Wollenberg KC, Vieites DR, Glaw F, Vences M, BMC Evol Biol 2011 11 1 217 10.1186/1471-2148-11-217 21777445
68. Signals of recent spatial expansions in the grey mouse lemur (Microcebus murinus). Schneider N, Chikhi L, Currat M, Radespiel U, BMC Evol Biol 2010 10 1 105 10.1186/1471-2148-10-105 20412584
69. Latitude drives diversification in Madagascar's endemic dry forest rodent Eliurus myoxinus (subfamily Nesomyinae). Shi JJ, Chan LM, Rakotomalala Z, Heilman AM, Goodman SM, Yoder AD, Biol J Linn Soc 2013 110 3 500 517 10.1111/bij.12143
70. A chronology for late prehistoric Madagascar. Burney DA, Burney LP, Godfrey LR, Jungers WL, Goodman SM, Wright HT, Jull A, J Hum Evol 2004 47 1 25 63 15288523
71. Box 4. Butchered sloth lemurs. Perez V, Burney D, Godfrey L, Nowak-Kemp M, Evol Anthropol 2003 12 6 260
72. La destruction d'une flore insulaire par le feu: principaux aspects de la végétation à Madagascar, documents photographiques et notices, vol. 5. Humbert H, Tananarive, Madagascar: Impr. Moderne de l'Emyrne, G. Pitot et Cie 1927
73. Sur l'extinction des vertébrés subfossiles et l'aridification du climat dans le Sud-ouest de Madagascar. Mahé J, Sourdat M, Bulletin de la Société de Géologie de France 1972 14 295 309
74. Prehistoric overkill: the global model. Martin PS, Quaternary Extinctions: a Prehistoric Revolution Tucson: University of Arizona Press, Martin PS, Klein RG, 1984 354 403
75. Extinctions in Madagascar: the loss of the subfossil fauna. Dewar RE, Quaternary Extinctions: a Prehistoric Revolution Tucson: University of Arizona Press, Martin PS, Klein RG, 1984 574 593
76. Rates, patterns, and processes of landscape transformation and extinction in Madagascar. Burney DA, Extinctions in Near Time: Causes, Contexts, and Consequences New York: Springer Science+Business Media, MacPhee RDE, 1999 145 164
77. Distribution and morphological variation of Microcebus spp. along an environmental gradient in southeastern Madagascar. Rakotondranary SJ, Hapke A, Ganzhorn JU, Int J Primatol 2011 32 5 1037 1057 10.1007/s10764-011-9521-z
78. Habitat separation of sympatric Microcebus spp. in the dry spiny forest of south-eastern Madagascar. Rakotondranary SJ, Ganzhorn JU, Folia Primatol 2012 82 4-5 212 223
79. Varying patterns of coexistence of two mouse lemur species (Microcebus ravelobensis and M. murinus) in a heterogeneous landscape. Rakotondravony R, Radespiel U, Am J Primatol 2009 71 11 928 938 10.1002/ajp.20732 19676112
80. Fifty years of deforestation and forest fragmentation in Madagascar. Harper GJ, Steininger MK, Tucker CJ, Juhn D, Hawkins F, Environ Conservat 2007 34 4 325
81. Irwin MT, Wright PC, Birkinshaw C, Fisher BL, Gardner CJ, Glos J, Goodman SM, Loiselle P, Rabeson P, Raharison J-L: Patterns of species change in anthropogenically disturbed forests of Madagascar. Biol Conservat 2010, 143(10):23512362.