Diversification and reproductive isolation: cryptic species in the only New World high-duty cycle bat, Pteronotus parnellii

Abstract

Background: Molecular techniques are increasingly employed to recognize the presence of cryptic species, even among commonly observed taxa. Previous studies have demonstrated that bats using high-duty cycle echolocation may be more likely to speciate quickly. Pteronotus parnellii is a widespread Neotropical bat and the only New World species to use high-duty cycle echolocation, a trait otherwise restricted to Old World taxa. Here we analyze morphological and acoustic variation and genetic divergence at the mitochondrial COI gene, the 7 th intron region of the y-linked Dby gene and the nuclear recombination-activating gene 2, and provide extensive evidence that P. parnellii is actually a cryptic species complex. Results: Central American populations form a single species while three additional species exist in northern South America: one in Venezuela, Trinidad and western Guyana and two occupying sympatric ranges in Guyana and Suriname. Reproductive isolation appears nearly complete (only one potential hybrid individual found). The complex likely arose within the last~6 million years with all taxa diverging quickly within the last~1-2 million years, following a pattern consistent with the geological history of Central and northern South America. Significant variation in cranial measures and forearm length exists between three of the four groups, although no individual morphological character can discriminate these in the field. Acoustic analysis reveals small differences (5-10 kHz) in echolocation calls between allopatric cryptic taxa that are unlikely to provide access to different prey resources but are consistent with divergence by drift in allopatric species or through selection for social recognition. Conclusions: This unique approach, considering morphological, acoustic and multi-locus genetic information inherited maternally, paternally and bi-parentally, provides strong support to conclusions about the cessation of gene flow and degree of reproductive isolation of these cryptic species.

The Roles of Taxonomy and Systematics in Bat Conservation

“…Vouchers are necessary for any future work such as reassessments of the initial study or further extension of the initial work when new information or methods become available. Vouchers, including tissue samples, are especially necessary when species are cryptic or nearly so-some bat species can only be identified by minute morphological differences, (e.g., cranial characters, or in small vespertilionids, the baculum (penis bone) (Hill and Harrison 1987) or by molecular means (e.g., Clare et al 2013). Vouchers are also necessary to provide type specimens (minimally a holotype but preferably also paratypes) if a new species is discovered (ICZN 2012).…”

Rapid assessment of bat diversity in the biological station ‘Las Guacamayas’ (‘Laguna del Tigre’ National Park, Guatemala)

“…Previously considered a species in its own right, Pteronotus parnellii is now seen as a complex of species difficult to identify (Lewis-Orrit et al 2001, Dávalos 2006, Clare et al 2013, De Thoisy et al 2014, López-Wilchis et al 2016, López-Baucells et al 2017. Captured 18 times (11 males and seven females) and recorded at all capture sites, this species is the most commonly captured bat in the biological station.…”

“…This species complex was already known for the National Park thanks to the capture of several individuals (Bestelmeyer & Alonso 2000). The forearm measurements of our captured individuals, between 52.2 and 59.2 mm, cannot be used to differentiate species from the complex (Clare et al 2013). Based on the basis of our ultrasound recordings (30 series analysed and 100 calls measured), the species has a QFC with an average of 63.0 ± 1.7 kHz that varies between 61.8 and 63.8 kHz (e.g.…”

Quaternary Bat Diversity in the Dominican Republic

“…Morphological and molecular studies have demonstrated that this complex includes at least five species and perhaps more, only some of which seem to correspond to previously delimited subspecies (Gutiérrez and Molinari, 2008;clare et al, 2013). Because the holotype P. parnellii is from Jamaica and antillean populations are typically much smaller than mainland forms, it seems likely that the name P. parnellii properly applies to all these bats including those from Hispaniola.…”

“…Oleg's Bat Cave: 19 complete skulls, 6 dentaries. extant distribution: cuba, Jamaica, Puerto Rico, Hispaniola, Saint Vincent, and possibly trinidad and tobago (Dávalos and turvey, 2012;clare et al, 2013).…”