MORMOOPIDAE, Saussure, 1860

DÁVALOS, LILIANA M., 2006, The geography of diversification in the mormoopids (Chiroptera: Mormoopidae), Biological Journal of the Linnean Society 88 (1), pp. 101-118 : 109-111

BASAL UNITS IN THE MORMOOPIDAE

The species diversity of the mormoopids has been underestimated. Two hypotheses underlie competing assessments of species diversity. The first hypothesis assumes populations of widespread species as part of a continuum of differentiation that appears great at the extremes, but is only slight between adjacent groups ( Koopman, 1955). Although some populations are allopatric, it is assumed that gene flow among them exists or occurred until recently. Because morphological intergradation (used to infer gene flow) among insular and continental populations is not observed, the range of (non)resemblance permitted in a given species has been widened ( Smith, 1972).

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The assessment of sequence variation among putative units (subspecies) within the mormoopids ( Table 2 ) revealed multiple instances of characters that appear to be fixed in cytochrome b. These molecular data support a second hypothesis: gene flow between insular and continental populations appears to have ceased even before fully recognized biological species (e.g. P. gymnonotus and davyi ; Fig. 3B ) evolved into separate lineages. The subtle morphological differences dismissed under a presumption of gene flow provide evidence for the isolation and independent evolution of separate lineages in widespread species such as parnellii , davyi , and personatus . Because sampling sizes for molecular markers were small, these differences alone cannot provide species limits. In some instances, molecular character differences, high sequence divergence among presumed conspecifics (bottom two tiers of Fig. 2 ), distributional ranges that encompass broad areas separated by water and land barriers ( Table 1 , Fig. 1 ), and taxonomic limits based on morphological variation ( Smith, 1972) coincide and strengthen the hypothesis of evolutionary independence. These criteria ( Tables 1 and 2 ) apply to named island populations of P. parnellii : parnellii ( Gray, 1843) , pusillus ( Allen, 1917) , and portoricensis ( Miller, 1902) ; the continental P. parnellii ranging from Mexico to Guyana currently classified in the subspecies mexicanus ( Miller, 1902), mesoamericanus ( Smith, 1972), and rubiginosus ( Wagner, 1843) ; the currently recognized subspecies of P. davyi : davyi ( Gray, 1838) and fulvus ( Thomas, 1892) ; and subspecies of P. personatus : personatus ( Wagner, 1843) and psilotis ( Dobson, 1878) . Each of these populations should be considered as a species, named using the subspecies taxonomy. The name Pteronotus rubiginosus ( Wagner, 1843) precedes mexicanus and mesoamericanus, and applies to the continental bats in the P. parnellii lineage as described above (note that the status of fuscus and paraguanensis was not evaluated; Table 1 ). Both cytochrome b ( Table 2 ) and Rag 2 ( Lewis Oritt et al., 2001) showed differentiation in Mexican and Central American populations of P. psilotis . Further sampling is necessary to determine if characters are fixed because taxonomic conclusions derived from single molecular exemplars would be suspect.

Mitochondrial cytochrome b from samples of Pteronotus rubiginosus and P. personatus from northern South America west of Guyana is distinct from that sampled east of Guyana ( Suriname and/or French Guiana; Table 2 , Fig. 1 ). These character differences and attendant levels of sequence divergence had not been anticipated in the morphological study of Smith (1972). French Guianan specimens of P. parnellii can also be distinguished from those from the remainder of the range by their larger size ( Simmons & Voss, 1998). In Venezuela, P. paraguanensis appears to have become isolated as a result of breaks in the humid forest ( Gutiérrez, 2004). This mechanism might explain the differentiation observed, but greater geographical and character sampling is needed to investigate these (possibly) cryptic species, and test the possibility that accelerated rates of sequence evolution have led to this pattern (although this is unlikely, see Table 4 ).

In P. quadridens discontinuous variation in cytochrome b occurs between Cuba and Jamaica, and Hispaniola and Puerto Rico, rather than coinciding with the subspecies taxonomy that separates Cuban from other Greater Antillean bats ( Tables 1 , 2 ). These taxa are not elevated to species here, despite the possible geographical isolation by ocean barriers, because sampling was sparse, the molecular differentiation does not match subspecies boundaries based on morphology, and no differences were detected in Rag 2. For the purpose of estimating ancestral areas, each terminal that appears with a name in Figure 3 was treated as a separate taxon.

Figures

Figure 1. Map of the Caribbean and biogeographical hypotheses about the origin of mormoopids. According to Smith (1972), ancestral mormoopids dispersed from northern South America or southern Central America to Mexico/ Central America. From there, the ancestors of Greater Antillean mormoopids reached the West Indies through Cuba via Yucatán, or Jamaica via Honduras. Dispersal through these routes would explain the distribution of the single lineage comprising Pteronotus quadridens and macleayii (ancient), the species Mormoops blainvillei (less ancient), and the Caribbean populations of Pteronotus parnellii (most recent). Czaplewski & Morgan (2003) concur on the dispersal routes to the Caribbean, but propose that mormoopids colonized the islands early in their evolutionary history. From Mexico/Central America, mormoopids would have reached South America recently, after the closing of the Isthmus of Panama.

Figure 2. Scatter plot of uncorrected sequence divergence in cytochrome b against taxonomic rank. Taxonomy follows Smith (1972). Numerals indicate cytochrome b distance outliers: 1: with respect to Saccopteryx; 2: between Mystacina and Noctilio; 3: between Mormoops and Artibeus; 4: between Noctilio albiventris and Noctilio leporinus; 5: between Pteronotus davyi and Pteronotus gymnonotus; 6: between currently recognized subspecies of Pteronotus quadridens, Pteronotus macleayii, and Mormoops megalophylla; and also between Pteronotus parnellii from Mexico, Guatemala and Honduras classified in the subspecies mesoamericanus and mexicanus; 7: between P. parnellii from Puerto Rico and Hispaniola, and among samples from Guyana, Mexico and Honduras; 8: between Pteronotus personatus from Suriname, and individuals from Venezuela and Guyana; 9: between P. parnellii individuals from French Guiana and Suriname; and 10: between P. parnellii individuals from Guyana, and Suriname and French Guiana.

Figure 3. A, strict consensus of eight most parsimonious cladograms resulting from analysis of cytochrome b (L = 1792 steps, consistency index = 0.439, retention index = 0.775). Numbers below branches are Bremer support values, above branches are percent of 1000 jackknife replicates. Names of outgroups are in bold; for sequence data, see Appendix. B, phylogram resulting from maximum likelihood analysis using a rate-constant GTR+I+Γ model of DNA evolution (–lnL = 9181.23). Numbers above or below branches are percent of 300 50% jackknife replicates, thicker lines indicate 100% jackknife support.