Pteronotus, Gray, 1838

Pavan, Ana C & Marroig, Gabriel, 2017, Timing and patterns of diversification in the Neotropical bat genus Pteronotus (Mormoopidae)., Molecular phylogenetics and evolution 108, pp. 61-69 : 63-66

3.2. Diversification times in the genus Pteronotus

The rising of Mormoopidae is estimated in the late Oligocene, ca. 32 Ma (95% HPD = 31–36.7 Myr). Divergence time of the Most Recent Common Ancestor (MRCA) of genus Pteronotus dates to the middle Miocene, around 16.1 Ma, with a confidence interval (95% HPD) ranging from 12.3 to 20.2 Myr. Diversification events giving rise to the main clades of Pteronotus are evenly distributed along the genus phylogeny. The first was the basal split between the ancestor of Clade 4 (subgenus Phyllodia ) and the branch giving rise to the other Pteronotus clades. Splitting between Clade 3 and the ancestor of Clades 1 and 2 also took place early in the genus evolutionary history (~ 13.9 Ma), followed by the separation of Clades 1 and 2 at 11.3 Ma. Emergence of closely related species started at the late Miocene, around 7.5 Ma, with differentiation between P. macleayi and P. quadridens within Clade 2, and extended through all Pliocene less than 3 Ma with cladogenesis within Clades 4, 3 and 1. Origin and diversification of most extant Pteronotus lineages is recent, occurring during the Pleistocene ( Fig. 1 and Table 2).

3.3. Ancestral geographic ranges

Results of the six biogeographic models implemented in BioGeoBEARS are presented in Table 3, which describes Log-likelihood values found for each of them. Comparative statistics show that DIVAj (LnL = ¯42.27) and DIVA (LnL = ¯44.07) models best fitted the data, indicating assumptions on geographic range evolution made by dispersal-vicariant method mostly satisfy patterns of geographic distribution of Pteronotus lineages. Implementation of DIVA model includes two free anagenetic parameters, d (dispersion rate/range expansion) and e (extinction rate/range retraction), and fixed cladogenetic parameters allowing equal probability of vicariance for all descendant size ranges, but disallowing subset sympatric speciation ( Matzke, 2013). The assignment of the free parameter J in the model, specifying weights for jump-dispersal events in the cladogenesis matrix, produced significant improvement of the biogeographic model (AICwt = 0.69 for DIVAj versus 0.31 for DIVA; Table 3). As previously shown for other islands groups ( Matzke, 2014), inclusion of the J parameter in the model was important to explain some biogeographic events in the genus Pteronotus , such as colonization of Caribbean islands.

The most probable states for the ancestral node ranges for the genus Pteronotus were estimated using the DIVAj model ( Fig. 2 ). Geographic range estimates of early nodes in the phylogeny had relatively low probabilities in all biogeographic models (data not shown), demonstrating higher uncertainty of biogeographic inferences. Area combinations displayed with black dashed lines in phylogeny nodes had frequencies smaller than 10% in the estimates, but that still are the most probable states amongst the 638 possible area combinations. The most probable alternative states of ancestral ranges according to DIVAj model are listed in Table S3.

According to the DIVAj model, the ancestor of Pteronotus inhabited a wide geographic area, ranging from Central America and Jamaica to the Amazon Region. An initial vicariant event split this population in the ancestral lineage of Clade 4 in South America and the ancestral lineage of Clades 1 + 2 + 3 in Central America (both ancestors could not have raised in CA because dispersal-vicariant model does not allow subset sympatric speciation). The ancestral population of Clade 4 later expanded its range into Central America, while ancestor of Clades 1, 2 and 3 diversified and dispersed to South America. In the subsequent cladogenesis event, between Clades 1 and 2, the first dispersal jump to Greater Antilles in the genus evolutionary history took place. The dotted-lined arrows in Fig. 2 highlight the shift in ancestral geographic ranges from Caribbean Coast and Central America to Jamaica and Cuba at Clade 2 ancestor. Diversification events within Clades 3 and 4 also required dispersal jumps, as displayed by the same arrows in the figure. Within Clade 4, both Amazon occupation by the ancestor of Clade 4C and the second colonization event in the Greater Antilles by the ancestor of Clade 4A were presumed to involve shifts in ancestral distributions. A similar scenario is estimated by the DIVA model ( Fig. S2 ), except that occupation of new areas occurred via anagenetic dispersal of ancestral populations instead of through jumps at cladogenesis events.

4. Discussion

4.1. Origin and diversification patterns in the genus Pteronotus

Our time-scale estimates suggest that early cladogenesis events within the genus Pteronotus occurred gradually, encompassing a large time range during the evolutionary history of this group. The age of the Most Recent Common Ancestor (MRCA) of genus Pteronotus was estimated to be between 12.3 and 20.2 Ma, which is old when compared to divergence of other bat genera ( Lim, 2008; Rojas et al., 2016; Velazco and Patterson, 2013). Despite this, the genus Pteronotus harbors a relatively small number of species, which are morphologically homogeneous in their skull and external characters ( Simmons and Conway, 2001). The lack of phenotypic variation confounded early species designations based solely on morphology, while this genus is characterized by deep genetic divergences among lineages ( Pavan and Marroig, 2016). Interestingly, the MRCA of the genus Pteronotus lived around 16 Ma, which represents just half of age of the MRCA of Family Mormoopidae , estimated to be at least 32 Myr old. This large interval of ca. 16 Myr between family and genus origins may imply the ancestor of Pteronotus underwent a long period of anagenetic evolution or, alternatively, that basal lineages filling this temporal gap became extinct later.

Biogeographic reconstruction of DIVAj model provides a scenario with both vicariant events and dispersal jumps to explain distributional patterns of extant Pteronotus lineages. This model proposes a widely distributed ancestor for the genus Pteronotus , which does not favor any of the current biogeographic hypotheses on the group origin ( Morgan and Czaplewski, 2012; Smith, 1972). It is important to highlight, however, that ancestral range estimates by DIVA model seeks to minimize dispersal-extinction costs ( Ronquist, 1997). Thus, it tends to reconstruct wide ancestral ranges at early nodes (which are directly related to the maximum number of areas settled) to explain distributional patterns of phylogeny tips ( Lamm and Redelings, 2009; Ree et al., 2005). In spite of this, it seems that founder event speciation was an important mode of lineage splitting in the genus Pteronotus , particularly within Clade 4.

Figures

Fig. 1. Maximum clade credibity tree with divergence estimates in the genus Pteronotus using fossil calibration.Bars correspond to the 95% High Posterior Density (HPD) time interval of each node. Bayesian Posterior Probabilities (BPP) of all nodes were higher than 0.95.

Fig. 2. Geographic range evolution in the genus Pteronotus. (a) Current distribution of genus Pteronotus (coloured map) with biogeographical areas scored for species presence/absence matrix.ME = Mexico;CA = Central America; CC = Caribean Coast of South America; LA = Lesser Antilles; AM = Amazon; CE = Brazilian Dry Diagonal:Cerrado and Caatinga; AF = Northern Atlantic Forest; JC = Jamaica and Cuba; HI = Hispaniola; PR = Puerto Rico. (b) Geographic range estimates with the highest marginal probabilities for Pteronotus ancestral nodes according to DIVAj model. Dashed-line borders indicate area combinations with probabilities smaller than 10% in the model, but still being the most probable state in that node among the 638 possible combinations. Curved arrows represent splits in the ancestral geographic ranges explained by vicariance; many of them were succeeded by anagenetic dispersal/extinction events, as highlighted by the linear black arrows; Dotted-line straight arrows highlight shifts in nodes geographic ranges due to dispersal jumps.