Phylogeny, time divergence, and historical biogeography of the South American Liolaemus alticolor-bibronii group (Iguania: Liolaemidae)

Abstract

The genus Liolaemus comprises more than 260 species and can be divided in two subgenera: Eulaemus and Liolaemus sensu stricto. In this paper, we present a phylogenetic analysis, divergence times, and ancestral distribution ranges of the Liolaemus alticolor-bibronii group (Liolaemus sensu stricto subgenus). We inferred a total evidence phylogeny combining molecular (Cytb and 12S genes) and morphological characters using Maximum Parsimony and Bayesian Inference. Divergence times were calculated using Bayesian MCMC with an uncorrelated lognormal distributed relaxed clock, calibrated with a fossil record. Ancestral ranges were estimated using the Dispersal-Extinction-Cladogenesis (DEC-Lagrange). Effects of some a priori parameters of DEC were also tested. Distribution ranged from central Perú to southern Argentina, including areas at sea level up to the high Andes. The L. alticolor-bibronii group was recovered as monophyletic, formed by two clades: L. walkeri and L. gracilis, the latter can be split in two groups. Additionally, many species candidates were recognized. We estimate that the L. alticolor-bibronii group diversified 14.5 Myr ago, during the Middle Miocene. Our results suggest that the ancestor of the Liolaemus alticolor-bibronii group was distributed in a wide area including Patagonia and Puna highlands. The speciation pattern follows the South-North Diversification Hypothesis, following the Andean uplift.

Keywords: Ancestral range; Andean uplift; Liolaemus; Lizards; Total evidence.

Figure 1. Map of South America showing the biogeographic regions used.

Biogeographic regions of Morrone (2001) employed in DEC analyses. (A) Desierto Peruano Costero, (B) Puna, (C) Yungas, (D) Atacama, (E) Coquimbo, (F) Prepuna, (G) Monte, (H) Chaco, (I) Pampa, (J) Santiago, (K) Maule, (L) Patagonia Central, and (M) Patagonia Subandina.

Figure 2. Congruence between the Maximum Parsimony (MP) and Bayesian Inference (BI) analyses

* Some members of the L. lemniscatus clade is recovered as a sister group of the L. walkeri clade under MP. Numbers above nodes correspond to Posterior Probabilities (Only Probabilities over 0.95 are shown). Numbers under nodes correspond to Symmetric Resampling values.

Figure 3. Topology recovered with Bayesian Inference.

Numbers above nodes correspond to Posterior Probability values (only values over 0.95 are shown).

Figure 4. Topology recovered with Maximum Parsimony.

Numbers above nodes correspond to Symmetric Resampling values (only values over 60 are shown). Note that the L. lemniscatus is paraphyletic and some species of this group are nested inside the L. walkeri clade.

Figure 5. Times of divergences estimates for the L. alticolor-bibronii group, under BI topology

Ultrametric tree scaled in Myr. Numbers and horizontal bars on nodes represent posterior probabilities values and 95% credibility intervals. (A) L. bibronii sensu stricto group; (B) L. robertmertensi group; (C) L. gracilis group; (D) L. walkeri clade; C + D: L. alticolor-bibronii group (E) L. gravenhorsti group; (F) L. lemniscatus group.

Figure 6. Times of divergences estimates for the L. alticolor-bibronii group, under MP topology.

Ultrametric tree scaled in Myr. Numbers and horizontal bars on nodes represent posterior probabilities values and 95% credibility intervals. (A) L. bibronii sensu stricto group; (B) L. robertmertensi group; (C) L. gracilis group; (D) L. walkeri clade; C + D: L. alticolor-bibronii group (E) L. gravenhorsti group.

Figure 7. Ancestral area of distribution (unconstrained adjacency matrix-BI topology).

The analysis was run by randomly dividing the entire time span of evolution of the Liolaemus alticolor- bibronii group in three periods (18–5.5 Myr; 5.5–1.25 Myr; 1.25 Myr-present). Pie charts of each node depict the relative probabilities of ancestral area/ranges (showed in Legend). Letters above nodes represent ancestral ranges. Circles around pie charts represent events: blue circle: dispersal event; green circle: vicariance. See material and methods for area names shown in South America map. Time axis (in Myr) is annotated with major geological events.

Figure 8. Ancestral area of distribution (unconstrained adjacency matrix-MP topology).

The analysis was run by randomly dividing the entire time span of evolution of the Liolaemus alticolor- bibronii group in three periods (18–5.5 Myr; 5.5–1.25 Myr; 1.25 Myr-present). Pie charts of each node depict the relative probabilities of ancestral area/ranges (showed in Legend). Letters above nodes represent ancestral ranges. Circles around pie charts represent events: blue circle: dispersal event; green circle: vicariance. See material and methods for area names shown in South America map. Time axis (in Myr) is annotated with major geological events.