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Geographic dispersion of Phyllostomidae family (Chiroptera) based on Cytochrome b sequences

Dispersão geográfica da família Phyllostomidae (Chiroptera) baseado nas sequências do cifocromo b

Dispersión geográfica de la familia Phyllostomidae (Chiroptera) basada en las secuencias del cifocromo b

^ISeção de Arbovirologia e Febres Hemorrágicas, Instituto Evandro Chagas/SVS/MS, Ananindeua, Pará, Brasil
^IISeção de Meio Ambiente, Instituto Evandro Chagas/SVS/MS, Ananindeua, Pará, Brasil. Universidade Federal do Pará, Belém, Pará, Brasil
^IIICentro de Inovações Tecnológicas, Instituto Evandro Chagas/SVS/MS, Ananindeua, Pará, Brasil. Laboratório de Biologia Molecular, Centro de Ciências Biológicas e da Saúde, Universidade Estadual do Pará, Belém, Pará, Brasil

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ABSTRACT

Keywords: Phylogeography; Chiroptera; Genes; Cytochromes b.

RESUMO

A ordem Chiroptera é uma das espécies de mamíferos mais bem sucedidas com uma grande distribuição geográfica. Essa ordem foi tradicionalmente dividida em duas subordens, Microchiroptera e Megachiroptera, e a família Phyllostomidae está incluída na primeira. No entanto, estudos com análise molecular mostram uma classificação diferente em duas subordens distintas: Yangochiroptera e Yinpterochiroptera. Os estudos com várias espécies descrevem uma grande dispersão desses animais da América Central para a América do Sul e espécimes de vários lugares, a criação de novos cariótipos e sequências de nucleotídeos diferentes, especialmente no gene citocromo b amplamente conhecido. Neste estudo, analisou-se uma dispersão filogeográfica da família Pyllostomidae usando o gene mitocondrial citocromo b, um possível padrão de dispersão para essa família e novas propostas evolutivas. Todas as sequências foram obtidas a partir da base de dados on-line (GenBank), a análise e a formação de árvores filogenéticas foram realizadas pelos métodos de máxima parcimônia e de máxima verossimilhança. Foram observados alguns padrões de dispersão de espécies do gênero Carollia e Glossophaga na análise individual e outro padrão de dispersão de espécies do sul ao oeste. Porém, na análise geral, um padrão de dispersão para o norte do Continente Americano foi evidenciado para a família, depois da América do Sul à América Central, apesar de muitos acidentes geográficos causarem especiação de alguns gêneros, tais como o isolamento das montanhas dos Andes. Uma análise mais aprofundada, com um maior número de amostras de diferentes locais, deve ser feita para confirmar esta teoria.

Palavras-chave: Filogeografia; Quirópteros; Genes; Citocromos b.

RESUMEN

El orden Chiroptera es una de las especies de mamíferos de mejores resultados y con una gran distribución geográfica. Ese orden ha sido tradicionalmente dividido en dos subórdenes, Microchiroptera y Megachiroptera, y la familia Phyllostomidae está incluida en la primera. Sin embargo, estudios con análisis molecular muestran una clasificación diferente en dos subórdenes distintas: Yangochiroptera e Yinpterochiroptera. Los estudios con varias especies describen una gran dispersión de esos animales de América Central para América del Sur y especímenes de varios lugares, la creación de nuevos cariotipos y secuencias de nucleótidos distintos, especialmente en el gen citocromo b ampliamente conocido. En este estudio se analiza una dispersión filogeográfica de la familia Pyllostomidae usando el genoma mitocondrial citocromo b, un posible estándar de dispersión para esa familia y nuevas propuestas evolutivas. Todas las secuencias se obtuvieron a partir de la base de datos online (GenBank), el análisis y la formación de los árboles filogenéticos se realizaron por los métodos de máxima parsimonia y máxima verosimilitud. Se observaron algunos estándares de dispersión de especies del género Carollia y Glossophaga en el análisis individual y otro estándar de dispersión de especies del sur al oeste. Sin embargo, se evidenció en el análisis general, un estándar de dispersión hacia el norte del Continente Americano para la familia, después de América del Sur a América Central, a pesar de que muchos accidentes geográficos causan la especiación de algunos géneros, como el aislamiento de las montañas de los Andes. Un análisis más profundo, con un número de muestras de diferentes locales más grande debe hacerse para confirmar esta teoría.

Palabras clave: Filogeografía; Quirópteros; Genes; Citocromos b.

Bats, classified in the order Chiroptera (cheir = hand; pteron = wing), are the only mammals that exhibit morphological and physiological adaptations for true powered flight. Their membranous wings extend between fingers, constituting dactilopatagium, which allow them flap the wings and fly. Other features that distinguish bats are the presence of membranes in the lower limbs called uropatagium and above the lower limbs, called protopatagium^1,2.

The order has a wide geographical distribution, found on all continents, except in the Polar Regions. Among all continents, the South and Central America have the high diversity of species, in contrast to North America and northern Eurasia, which have a low diversity, due to increasing latitude and consequently reducing the temperature^3,4,5,6,7,8.

Over the decades, the classification of Chiroptera changed several times. The traditional classification recognized two suborders: Megachiroptera and Microchiroptera. Simmons⁹ has described a total of 18 families, 202 genera and 1,120 species.

The Megachiroptera is composed of a single family Pteropodidae, which has 190 species divide into four subfamilies: Pteropodinae, Harpyonycterinae, Nyctimeninae and Macroglossinae. Microchiroptera has 930 species divide into 17 families: Rhinolophidae, Hipposideridae, Megadermatidae, Rhinopomatidae, Phyllostomidae, Craseonycterinae, Emballonuridae, Nycteridae, Myzopodidae, Mystacinidae, Molossidae, Vespertilionidae, Mormoopidae, Noctilionidae, Furipteridae, Thyropteridae and Natalidae⁹.

In contrast to the traditional morphological classification, recent cytogenetic and molecular studies have proposed a different classification for bats. Some authors have divided the order into two new suborders Yangochiroptera (consisting of Microchiroptera, except Rhinopomatidae, Rhinolophidae and Megadermatidae) and Yinpterochiroptera (consisting of Megachiroptera and families Rhinopomatidae, Rhinolophidae and Megadermatidae)^10,11,12.

Among the several bat families that have been found in Brazil, the most common is the Phyllostomidae (from greek: phyllo = leaf + stoma = mouth), which is composed by a variety of bats that have different eating habits, such as insectivorous, frugivorous, carnivorous, herbivorous, nectarivorous, omnivorous and hematophagous^2,13.

The Phyllostomidae family is divided into seven subfamilies: Desmodontinae, Glossophaginae, Phyllostominae, Carolliinae, Stenodermatinae, Phyllonycterinae and Brachyphyllinae and more than 160 species are grouped in 48 genera⁹. The family was classified in Microchiroptera or Yangochiroptera^10,11,12.

The main morphological feature is an appendix in the format of a shaped spearhead, also called "leaf nose", except for Desmodontinae subfamily, and the species Cenfurio senex (the structure is reduced or absent). Its species are mostly adapted to low altitudes in the tropical and subtropical regions of the New World⁹. They can be found from the Southeastern United States to northern of Argentina¹³.

At the beginning of this century, there was a large number of taxonomic and systematic revisions in several groups of bats present in Brazil, proposing new classifications between families and genera of Chiroptera^{9,14,15,16,17}.

Since the 1970s, several molecular techniques, such as electrophoresis, polymerase chain reaction (PCR), DNA sequencing, proteomics and others were used in several studies, mainly in phylogenetic^14,21,22. These techniques can be used to analyze nuclear DNA and DNA from organelles, allowing the measurement of phylogeographic parameters, gene flow and it's inter and intraspecific historical relationships^14,17,21.

Currently, one of the most widely used markers for studying phylogeny and phylogeography is the mitochondrial DNA (mtDNA), which is circular, haploid and matrilineal (maternal inheritance pattern). It is found in the mitochondrial lumen with thousands of copies per cell, almost all of the genome is involved in coding functions and the existence of pseudogenes, introns and repetitive DNA is rare^23,24. One of the suitable features for the genetic analysis is the ability to accumulate base substitutions, insertions and deletions at a rate of five to ten times faster than nuclear DNA, due to low replication fidelity, no repair mechanisms, corrosive oxygen-rich environment and no DNA compaction²³. The phylogeny based on mtDNA allows a good description of the geographical distribution, genetic distances and divergence times between lineages¹.

The most widely used marker is the Cytochrome b gene that has one of the best resolutions for phylogenetic studies in mammals with divergence times from four to 44 million years^1,25. The gene contains codons with fast and slow evolution, conserved regions and variable regions²⁶. It has been widely used in analyzes that involves geographic distribution of genetic lineages, evolution, reproductive isolation, origin, distribution, biodiversity maintenance and the emergence of new species²⁷. Based on its variability, Cytochrome b gene is considered appropriate to elucidate relationships to a genus level, the saturation may complicate at higher taxonomic levels¹⁴.

Phylogeography studies using molecular data (usually mtDNA and microsatellite) can propose a geographic evolution (based on vicariance, diversification of species and patterns of migration) and demographic history (fixation of species, population growth and decline)³.

Among several works about the phylogeography of the Phyllostomidae family, little is known of its evolution, dispersal and establishment of the species, in general perspective. Most studies use only a few genera, species or small groups, never with a general group, using various genera^3,4,5,6,7,8.

In Phyllostomidae, only Leptonycteris curasoae, Leptonycteris nivalis, Choernycteris mexicana and Platalina genovensium needs a migratory behavior. In other families, few species have this behavior and most are classified in the Vespertillionidae family²⁸. This migration, in some species, may be greater in females than in males and changes may occur especially in Neotropics wet and dry seasons²⁹. What differentiates bats from birds, in the migratory aspect, is that bats hibernate in caves and mines during the winter and birds migrate to different locations to get out of the food shortages and climate change^30,31.

Bats from North America and South America have been exchanging genetic information and fauna over a millions years, compounding the tropical fauna of mammals in the Americas⁵. The dispersion has occurred in regions that had a higher amount of food, especially in autumn season³².

Thus, the aim of this study was to analyze the evolutionary and phylogeographic dispersal involving species of bats of the Phyllostomidae using the mitochondrial gene, Cytochrome b, and suggesting a possible dispersion pattern for the family.

All procedures were performed at Instituto Evandro Chagas in the Centro de Inovações Tecnológicas. The DNA sequences of Cytochrome b gene were obtained directly from GenBank (NCBI) (http://www.ncbi.nlm.nih.gov/genbank). It was retrieved 50 complete Cytochrome b sequences of 1,140 bp for a variety of localities throughout the American Continent (Table 1). It was only used sequences with the locality referred in the original articles.

The numbers of retrieved sequences were low because many sequences were not in the referenced article, others have not been published in articles and others did not mention the sites that the specimens were captured.

PHYLOGENETIC ANALYZES

In order to observe genetic variations, the nucleotide sequences were aligned and compared using BioEdit 7.0 software. For phylogenetic tree formation, it was used the maximum parsimony and maximum likelihood methods. Analysis were performed considering all nucleotides and codons substitutions with heuristic search in PAUP 4.0b10 software using the tree bisection-reconnection (TBR). The bootstrap value was expected in one thousand replications using the heuristic test. In the maximum likelihood analysis were used GTR nucleotide substitution models and TBR with gamma frequencies chosen by software J Model Test 2.1.3. Both analysis were based on the parameters described in Baker²¹.

It was used the genus Mormoops from the Mormoopidae as outgroup because it is considered one of the closest to the Phyllostomidae according to Baker et al²¹ and Jones et al¹⁷. Intraspecific analysis were performed for each species and interspecific with all genera retrieved from GenBank (Table 1).

RESULTS

In the maximum parsimony analysis, from 1,140 characters, 651 were invariant, 455 were informative and 34 uninformative.

It could be observed seven distinct groups without evolutionary information between them, but internally for the genus Artibeus, it was observed that Artibeus jamaicensis had basal status in relation to Artibeus lituratus. The specimen of Carollia brevicauda had basal status in relation to specimens of the same species and to Carollia pespecillata. Regarding the species Ectophylla alba, the specimen that was obtained from Panama had a basal status compared the ones in Costa Rica. The species Glossophaga commissarisi, from Panama also has basal status relative to all other species from Glossophaga genus (Figure 1).

In groups 5, 6, 7 and 8 the specimens with basal status are: Uroderma bilobatum from Honduras, Vampyrodes caraccioli from Peru, Vampyressa thyone from Panama and Micronycteris megalotis from Ecuador (specifically in El Oro, Puyango, Petrified Forest), respectively (Figure 2).

Regarding the analysis by maximum likelihood, three groups were formed, one with basal status in the family, having the specimens of Micronycteris megalotis, following two distinct groups composed of group 1 (with Tonatia, Glossophaga and Carollia) and group 2 by the remaining genus, with the most basal status for Ectophylla alba.

Artibeus jamaicensis - It was analyzed specimens from two different localities (Suriname and Ecuador). In maximum parsimony and maximum likelihood, the species was dispersed from East to West of South America, in which the specimens from Ecuador are more derived in the phylogenetic analysis than from Suriname.

Artibeus lituratus - It was analyzed specimens from two different localities (St. Vincent and the Grenadines and Ecuador). In maximum parsimony and maximum likelihood, the species were dispersed from East to West and to the South of South America, and the specimens of Ecuador are more derived than those of Saint Vincent and the Grenadines.

Carollia brevicauda - Specimens from three different locations were analyzed (Peru, Panama and Venezuela). In maximum parsimony and maximum likelihood, the species were dispersed from South to North of America, and the specimens of Venezuela are more derived than those from Panama and these are more derived than those from Peru.

Carollia castanea - Four different locations were analyzed (Peru, Ecuador, Bolivia and Panama). In maximum parsimony the specimens located in Ecuador are more basal, followed by two derived groups, one consisting of specimens from Bolivia and Peru and another consisting of specimens from Panama. In contrast, the maximum likelihood showed different results, that specimens from Peru were more basal in the phylogenetic tree, followed by specimens from Bolivia, Ecuador and Panama (Figure 2).

Carollia perspicillata - Specimens from five different locations were analyzed (Brazilian Amazon, Minas Gerais, Brazil, Mexico, Ecuador and Suriname). In parsimony and maximum likelihood the specimens located in Brazil (Minas Gerais) are more basal, followed by two derived groups, one consisting of specimens of the Brazilian Amazon, Mexico and Suriname and another group consisting of specimens from Brazilian Amazon and Ecuador (Figure 2).

Ectophylla alba - It was analyzed specimens from two different localities (Panama and Costa Rica). In parsimony and maximum likelihood, the specimens located in Panama are basal, followed by specimens from Costa Rica. Showing dispersion towards the North to Central America.

Glossophaga soricina - Specimens from six different locations were analyzed (Panama, Paraguay, Venezuela, El Salvador, Mexico and Jamaica). In parsimony and maximum likelihood, the specimens located in Venezuela are basal, followed by specimens from Paraguay, Panama, El Salvador, Jamaica and Mexico, suggesting dispersion towards the north, from South America to North America (Figure 2).

Mesophylla macconelli - Specimens from four locations were analyzed (Ecuador, Bolivia, Colombia, French Guiana). In maximum parsimony, two sister groups assembled, one with specimens from Bolivia and Colombia with the same degree of phylogenetic relatedness and another group showing specimens from French Guiana and Ecuador, which are more derived. Regarding the analysis by maximum likelihood, the specimens from Ecuador are basal, followed by specimens from French Guiana, Bolivia and Colombia (most derived).

Platyrrhinus dorsalis - It was analyzed specimens from two different localities (Bolivia and Ecuador). In parsimony and maximum likelihood, the species have spread to Northern of South America, in which the specimens of Bolivia are more derived than the specimens from Ecuador.

Uroderma bilobatum - Specimens from three countries were analyzed (Honduras, Panama and Ecuador). In parsimony and maximum likelihood, the species have spread from Southern Central America to South America, where the specimens from Honduras are more basal, followed by specimens from Panama and Ecuador (both in the same degree of phylogenetic relatedness).

Vampyressa thyone - In maximum parsimony, the species showed dispersion to the North of Central America, from Panama to Costa Rica. However, analysis by maximum likelihood was different, North to South, from Costa Rica to Panama.

Vampyrodes caraccioli - Three specimens were analyzed in Peru, Trinidad and Tobago and Brazil. In parsimony and maximum likelihood, dispersion followed from Peru to Trinidad and Tobago and Brazil.

DISCUSSION

In the general analysis by maximum parsimony, it was noticed the most basal status of the specimen Carollia brevicauda from Peru (Cuzco) comparing specimens of C. perspicillata and C. brevicauda presented in Venezuela, proposing a possible origin of these specimens from the specimen of southern (Peru). A spread of these specimens could be possible to the north of the American Continent and eastward Brazil. It was found the same analysis result for genera Glossophaga, Ectophylla, Vampyrodes, Vampyressa and, thus, proposing a dispersion pattern to the north in several species of that family (Figure 1).

The Andes may also have influenced in species that have affinity for high altitudes. Kunz and Pena⁴³ described the presence of Mesophylla macconelli in regions with altitude up to 1,032 m, Baker and Clark⁴⁴ described Uroderma bilobatum to 1,800 m and Lewis and Wilson⁴⁵ described Vampyressa pussila in 1,500 ft, among other species that also have some affinity with high altitudes.

The possible location and dispersion of Glossophaga may have been influenced by their ecology. For example, Glossophaga commissarisi is in a variety of habitats, such as rainforests, subtropical savannas and others. Another example is Glossophaga soricina according to their habitat and time of year, they may have a variable eating behavior, such as those in Mexico, that their feeding habits is mainly of nectar and pollen from April to June, then they change their feeding behavior to insectivorous. Alvarez et al⁴⁶ has also described eating behavior of nectar and pollen during the dry season in Panama and eating fruits in the wet season.

Hoffmann and Baker⁵ reported the emergence of the Isthmus of Panama as one of the factors of the dispersion to the North America, which was confirmed by studies with terrestrial mammals. The authors have also reported that the same situation may have happened with the bats, they might have taken advantage of the Isthmus "bridge" for dispersal between the continents. However, the same authors have mentioned that the phylogenetic variation in Carollia may have occurred by vicariance with the rise of the Andes mountains, preventing the spread of these bats and isolating individuals on the other side of the Andes. The same idea can be inferred for bats from other groups that may have this dispersion pattern to North. In this present study, Carollia perspicillata and C. castanea showed the same pattern of dispersal to the North of the American Continent, and C. castanea seemed to have a distribution along the Andes to Panama (Figures 2A, 3A, 2B and 3B), it can be possible due to an affinity to high altitudes, as previously mentioned for other species. However, it was also noticed similarities with the dispersion pattern to the North towards Panama and South, and another pattern towards Peru and Bolivia, as shown in figure 3, which differs from the idea of isolating of Carollia by the Andes.

The same pattern of vicariance may have occurred with Uroderma bilobatum, that has presented dispersion to Ecuador in the Andes Region, with the specimens from Panama as a sister group.

Other species such as Artibeus jamaicensis have dispersed to the West, probably because of better habitat with the emergence of forest refuges during the Pleistocene, causing several species disperse to new habitats in search of food, as occurred with the genus Carollia⁵. A good example of vicariance is the most basal status Artibeus lituratus present in St. Vincent and the Grenadines, which may have been a case of isolation, caused for the formation of islands.

Regarding the species Platyrrhinus dorsalis, Velazco and Patterson⁸ describe that the ancestor of the genus Platyrrhinus may have arisen in the South of the Amazon River in Brazil and dispersed towards the Andes and the Amazon basin, originating several new species of the genus. According to these authors, the species were found in the Northern Andes, occupying the area of Ecuador, following the North to Venezuela. However, in our analysis we found evidence of a possible spread North to Venezuela.

The preference for specific types of habitat of various species may also influence the Phyllostomidae dispersion. Some species prefer humid and wet habitats, like the Amazon forest and other tropical forests, for exemple, Artibeus jamaicensis, Mesophylla maconelli, Platyrrhinus dorsalis and Vampyrodes caraccioli^47,48,49. Others species, as example Uroderma bilobatum, prefer certain types of foods such as figs obtained in high trees of tropical forests⁴⁴.

CONCLUSION

It can be concluded that the Phyllostomidade family, in general, may have a dispersion pattern on the American Continent, it can be noticed that several species, in intraspecific analysiss, have a possible pattern, in the North America, as Carollia brevicauda, C. castanea, C. perspicillata, Glossophaga comissarisi and G. soricina or to the South, as Uroderma bilobatum and Vampyrodes caraccioli. Regarding the other species analyzed, it cannot be suggested a dispersion pattern, because the analisis presented a random dispersion or few specimens from different and distant localities.

Many other studies work at genus and species level, rarely at family level, due to lack of specimens from distant and different localities. Here it was performed an analysis of GenBank sequences for a possible dispersion theory to the North of the American Continent for Phyllostomidae family. The reduced number of retrieved sequences were low because of the lack of published sequences with its exact location of the specimen. However, the sequences obtained were really important due to the distinct and distant locations and features that can prove other dispersion theories, as the vicariance occurred by the emergence of the Andes Mountains. Thus, it concludes that the family may have a dispersion pattern (probably to the North), however other analysis must be performed in the future, as phylogenetic regression, molecular clock and the discovery of new sequences at other localities in the American Continent.

ACKNOWLEDGENTS

To Clayton Lima and the Centro de Inovações Tecnológicas, Arbovirologia e Febres Hemorrágicas and Meio Ambiente sections from Instituto Evandro Chagas and the Universidade Federal do Pará.

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Correspondence / Correspondência / Correspondencia:
Gustavo Moraes Holanda
Rua Antonio Barreto, 747. Bairro: Umarizal
CEP: 66055-050 Belém-Pará-Brasil
Phone #: +55 (91) 8757-2970
E-mail: holandagm@gmail.com

Received / Recebido em / Recibido en: 10/1/2012 ]]> Accepted / Aceito em / Aceito en: 19/6/2012