Phylogenetic relationships and species delimitation in the genus Pteronotus (Chiroptera: Mormoopidae)
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1 VIII ENCONTRO BRASILEIRO PARA O ESTUDO DE QUIRÓPTEROS EBEQ "Ferramentas para delimitação de espécies e a diversidade de morcegos na Região Neotropical Phylogenetic relationships and species delimitation in the genus Pteronotus (Chiroptera: Mormoopidae) ANA CAROLINA PAVAN
2 NATURAL HISTORY Family Mormoopidae: Insectivores Neotropical range Geographic overlap among species Humid tropical forest to arid subtropical forest and scrubland Large colonies
3 CLASSIFICATION 2 genera: Pteronotus Gray, 1838 and Mormoops Leach, species: Pteronotus parnellii Pteronotus paraguanensis Pteronotus personatus Pteronotus macleayi Pteronotus quadridens Pteronotus gymnonotus Pteronotus davyi 3 fossil species: Pteronotus pristinus Mormoops magna New genus and species Mormoops megalophylla Mormoops blainvillei P. parnellii
4 Taxonomic history Smith (1972) Chilonycterinae Mormoopidae Geographic variation: Smith (1972) 21 subspecies: 17 in Pteronotus Linares & Ojasti (1974) P. p. paraguanensis Gutierrez & Molinari (2008) P. paraguanensis
5 Geographic variation in Pteronotus Species Subspecies Geographic range P. p. parnellii Cuba and Jamaica P. p. pusillus Dominican Rep. and Haiti P. p. gonavensis Gônave island, Haiti P. p. portoricensis Puerto Rico P. p. mexicanus Sonora and Tamaulipas to Oaxaca and Veracruz, Mexico Pteronotus parnellii P. p. mesoamericanus Southern México and pacific coast of Central America to Panama P. p. fuscus Caribbean coast of Colombia and Venezuela, north of Orinoco river Pteronotus paraguanensis Pteronotus personatus Pteronotus davyi Pteronotus gymnonotus Pteronotus macleayi Pteronotus quadridens P. p. rubiginosus From Honduras southward along the Caribbean coast of Central America; Trinidad; Amazonian lowlands and Guiana Shield, south of Venezuela, Peru and Central Brazil --- Paraguaná peninsula, Venezuela P. p. psilotis Caribbean Coast of Honduras and El Salvador to Sonora and Tamaulipas, Mexico P. p. personatus Central Brazil to pacific coast of Costa Rica P. d. fulvus Caribbean Coast of Honduras and El Salvador to Sonora and Tamaulipas, Mexico P. d. davyi Caribbean Coast of South America and Lesser Antilles to south of Nicaragua P. d. incae Peru --- Central Brazil to Veracruz, Mexico P. m. macleayi Cuba P. m. griseus Jamaica P. q. quadridens Cuba P. q. fuliginosus Jamaica, Haiti, Dominican Rep., Puerto Rico
6 Recent studies Simmons & Conway (2001) Gutierrez and Molinari (2008) Guevara-Chumacero (2010) Lewis-oritt et al. (2001) Davalos (2006) Borisenko et al. (2008) Clare et al. (2011, 2013) De Thoisy et al. (2014) Hidden diversity
7 Genus Pteronotus Cryptic diversity Disjunct geographic range Molecular variation x morphological variation GOALS: Phylogenetic relationships in Pteronotus Cranial morphometrics Diversity and Species delimitation
8 Molecular Systematics
9 MATERIAL & METHODS 411 tissue samples P. parnellii = 247 P. personatus = 57
10 P. gymnonotus = 47 P. davyi = 28
11 P. quadridens = 24 P. macleayi = 8
12 MATERIAL & METHODS Six molecular markers Marker Gene / Region Fragment length Transmission System CITB Cytochrome b 1140pb Mitochondrial CO1 Cytochrome Oxidase 1 651pb Mitochondrial PRKC1 Protein-kinase C 462pb intron - autossomic STAT5A Signal transducer and activator of transcription 5A 605pb intron - autossomic DBY Ddx3y / DEAD box RNA helicase Y 510pb intron cromossome Y RAG2 Recombination Activating Gene 2 804pb exon- autossomic
13 MATERIAL & METHODS Molecular data analysis Edition and alignment: Geneious V.7.1 and MEGA6 Evolutionary models: PartitionFinder v Phylogenetic inferences: Mr. Bayes (BI), Garli 2.0 (ML), TNT v.1.1 (MP) Species tree: *BEAST v.1.8 Additional softwares: Tracer v.1.6, TreeAnnotator v.1.8, FigTree v.1.4 e DensiTree v
14 mtdna Outgroup Outgroup 1 / 98 0,89 / 62 0, / % 1 / 1 / 92 13% 4-9% 7% 1 / / 80 1 / 97 1 / 100 0,93 / * 0, / 52 1 / / / 92 1 / 38 1 / / / / / / / 48 1 / 92 1 / 84 1 / / 89 1 / / 68 Central America 1 / 80 Guatemala Central Brazil, Guiana Shield Jamaica Greater Antilles Lesser Antilles Guiana South America Brazilian amazon, Guiana Shield Hispaniola Puerto Rico Mexico Guatemala to Brazil Mexico Central America Greater Antilles Pteronotus gymnonotus P. d. davyi Pteronotus davyi P. d. fulvus Pteronotus quadridens Pteronotus macleayi P. p. personatus Pteronotus sp3 Pteronotus personatus Pteronotus sp2 P. p. psilotis P. p. rubiginosus P. p. pusillus P. p. portoricensis P. p. parnellii Pteronotus parnellii Pteronotus sp1 P. p. mesoamericanus P. p. mexicanus Clade 1 Clade 2 Clade 3 Clade / 97 1 / 91 St. Vicent & Grenadines Venezuela, St. Vicent & Grenadines P. p. fuscus Outgroups Outgroups 0.03 BI e ML Outgroup Outgroup MP 6.0
15 5 genes Complete Outgroup Outgroup Outgroup Outgroup Outgroup Mexico to Brazil P. gymnonotus B Clade 1 Clade 2 Clade 3 Clade 4 Lesser Antilles Central America Greater Antilles Cuba, Jamaica South America P. davyi P. quadridens P. macleayi A1 A2 B A A Basal relationships Guatemala P. personatus Guatemala Mexico B BI ML MP Central Brazil to Guyana Shield Brazilian Amazon to Guyana Shield A1 A2 BPP> 0.95; boot> 90% 0.80< BPP< 0.95; 70%<boot< 90% 50%<boot< 70% Jamaica Hispaniola Porto Rico Central America Mexico P. parnellii B1 B2 C3 C1 Boot<50% Venezuela, St. Vicent & Grenadines Outgroup
16 Species tree Coalescent approach Agrees with phylogenetic inference
17 CONCLUSIONS Pteronotus is monophyletic 4 major clades 3 taxa with cryptic diversity: P. davyi: 2 lineages P. personatus: 2 to 4 lineages P. parnellii: 8 lineages Lineages and subspecies correspondence
18 Morphometrics and Species delimitation
19 MATERIAL & METHODS 1626 specimens 13 collections Taxon TOTAL Pteronotus parnellii 759 Pteronotus paraguanensis 2 Pteronotus personatus 278 Pteronotus davyi 253 Pteronotus gymnonotus 211 Pteronotus macleayi 45 Pternotus quadridens 77 Institution Locality Country MZUSP São Paulo, SP Brasil IEPA Macapá, AP Brasil UFMG Belo Horizonte, MG Brasil INPA Manaus, AM Brasil UFPE Recife, PE Brasil UFPB João Pessoa, PB Brasil AMNH New York, NY EUA TCWC College Station, TX EUA KUM Lawrence, KS EUA NMNH Washington, DC EUA FMNH Chicago, IL EUA LACM Los Angeles, CA EUA TTU Lubbock, TX EUA
20 ZB ZS MATERIAL & METHODS ZYGO ZI LD 22 landmarks 41 linear distances ZB BR ZS NA NSL PM PM IS OPI JP BA JP TS APET APET TS TSP TSP ZYGO MT PNS MT ZI BR LD NSL AS PT PM IS PEAM EAM ZYGO
21 MATERIAL & METHODS MANOVA: sexual dimorphism PCA: Principal Component Analysis DFA: Discriminant Function Analysis D²: Mahalanobis (morphological distance) R development core team SYSTAT 11
22 RESULTS Outgroup Outgroup Phylogeny: hypothesis grouping for morphometric investigation DFA Clade 1: P. davyi + P. gymnonotus Clade 2: P. macleayi + P. quadridens Clade 3: P. personatus Clade 4: P. parnellii P. d. incae P. gymnonotus P. d. davyi P. d.. fulvus P. q. quadridens P. q. fuliginosus P. m. macleayi P. m. griseus P. p. personatus Pteronotus sp2 P. p. psilotis P. p. rubiginosus Pteronotus sp1 P. p. parnellii P. p. pusillus P. p. portoricensis P. p mexicanus P. p mesoamericanus P. p fuscus Outgroup 0.4
23 (12%) (6%) Clade 1 P. davyi: 3 categories P. gymnonotus DF2 + P. incae fulvus gymnonotus incae Total Jackknifed classification matrix 2 1 davyi 1 0 fulvus gymnonotus incae % correct davyi LINHAGEM 86 0 fulvus SUBESPECIE davyi gymnonotus fulvus davyi incae gymnonotus fulvus incae Total 62 gymnonotus incae DF1 (88%) DF1 (92%) DF2 Classification matrix davyi fulvus gymnonotus incae % correct davyi
24 Clade 2 P. quadridens: 2 categories Classification matrix fuliginosus quadridens % correct fuliginosus quadridens Total Jackknifed classification matrix fuliginosus quadridens % correct fuliginosus quadridens Total P. macleayi: 2 categories Classification matrix griseus macleayi % correct griseus macleayi Total Jackknifed classification matrix griseus macleayi % correct griseus macleayi Total
25 Clade 3 P. personatus: 2 categories Classification matrix personatus Psilotis % correct personatus 95 1 psilotis Total Jackknifed classification matrix personatus psilotis % correct personatus psilotis Total
26 (15%) Clades 2 and DF DF1 (75%) LINHAGEM macleayii personatus psilotis quadridens
27 Clade 4 Classification matrix P. parnellii: fusc 7 categories meso mexi parn port pusi rubi % correct fuscus mesoamericanus mexicanus parnellii portoricensis pusillus rubiginosus Total Jackknifed classification matrix fusc meso mexi parn port pusi rubi % correct fuscus mesoamericanus mexicanus parnellii portoricensis pusillus rubiginosus Total
28 (17%) Clade 4 DF DF1(70%) + LINHAGEM fuscus mesoamericanus mexicanus parnellii portoricensis pusillus rubiginosus
29 Clade 4 Island x mainland Insular populations: discrete units Mainland populations: gradient High genetic divergence Echolocation as an additional evidence: mexicanus: 64kHz (Novick 1963) mesoamericanus: 62.1kHz (Clare et al. 2013) fuscus: 58.9kHz (Clare et al. 2013) rubiginosus: 53 khz (de Thoisy et al. 2014) Pteronotus sp1: 59 khz (de Thoisy et al. 2014)
30 Diversity in the genus Pteronotus
31 Clade 1: Four species P. fulvus? P. davyi P. incae P. gymnonotus
32 Clade 2: Two species P. macleayi P. quadridens
33 Clade 3: Two species P. psilotis P. personatus
34 Clade 4: Nine species P. parnellii P. mexicanus P. mesoamericanus P. portoricensis P. pusillus P. paraguanensis P. fuscus Pteronotus sp. P. rubiginosus
35 Taxonomic arrangement Mormoops Mormoops blainvillei Mormoops megalophylla Mormoops magna Mormoopidae Pteronotus Pteronotus Chilonycteris Pteronotus Chilonycteris Phyllodia Phyllodia Pteronotus davyi Pteronotus fulvus Pteronotus incae Pteronotus gymnonotus Pteronotus quadridens Pteronotus Pteronotus davyi macleayi Pteronotus gymnonotus Pteronotus parnellii Pteronotus portoricensis Pteronotus quadridens pusillus Pteronotus macleayi mexicanus Pteronotus personatus mesoamericanus Pteronotus fuscus Pteronotus Pteronotus parnellii paraguanensis Pteronotus Pteronotus pristinus rubiginosus Pteronotus sp1 Pteronotus pristinus Novo subgênero Pteronotus personatus Pteronotus psilotis
36 CONSIDERATIONS Intraclade diversification without clear morphological change Cranial variation agrees with molecular diversity Echolocation as a taxonomic tool in P. parnellii
37 AGRADECIMENTOS Gabriel Marroig & LEM/USP Pesquisadores e coleções científicas
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