Elachistocleis

Jowers, Michael J., Othman, Siti N., Borzée, Amaël, Rivas, Gilson A., Sánchez-Ramírez, Santiago, Auguste, Renoir J., Downie, J. Roger, Read, Morley & Murphy, John C., 2021, Unraveling unique island colonization events in Elachistocleis frogs: phylogeography, cryptic divergence, and taxonomical implications, Organisms Diversity & Evolution (New York, N. Y.) 21 (1), pp. 189-206 : 201-202

Elachistocleis phylogeography

Elachistocleis araios is the only species restricted to the Pacific versant of the Andes while E. panamensis and E. pearsei are found up to the Caribbean Sea. Our data suggest a northern expansion from Ecuador towards Colombia in the Late Oligocene to Early Miocene, a timing in agreement with new world microhylid radiations, believed to have started in the Oligocene in northern South America ( van der Meijden et al. 2007; de Sá et al. 2012). Until the recent discovery of E. araios ( Sanchez-Nivicela et al. 2020) , the basal positioning of E. panamensis pointed towards an Atlantic to Caribbean Colombian origin ( de Sá et al. 2012). Still, the ancestral position of both species suggests an Andean origin, in congruence with molecular studies to account for the Amazonian amphibian diversity ( Santos et al. 2014). The high genetic divergence of both ancestral species likely reflects allopatric events in the region, by the uplift of the Andes between ~40 and ~23 Mya, affecting the isolation of E. araios to the west. Also, E. panamensis expansion may have been constrained throughout the Late Miocene by a deep marine incursion draining to the west of their distribution, ending in the Caribbean region ( Santos et al. 2009; Hoorn et al. 2010; Kay 2015; Cordeiro Bicudo et al. 2019) ( Fig. 3 ).

The divergence between both major Elachistocleis clades corresponds to the Mid-Miocene. In the Llanos Basin, the first marine transgression covered the basin during the Early Miocene, between 19.1 to 17.2 Mya (lasting 0.9 My) and again in northwestern Amazonas between 18.0 and 17.8 Mya (lasting 0.2 My). A second much more prolonged transgression occurred in the Llanos Basin between 16.1 and 12.4 Mya (lasting 3.7 My) and its continuation towards the Amazonas /Solimões Basin between 14.1 and 13.7 Mya (continuing 0.4 My; Jaramillo et al. 2017). The timing of the last two marine transgressions fall exactly within our divergence time estimates of both clades and may suggest that during this period, the ancestors of the recovered clades were separated through vicariant events in the region. In accordance, the distribution of E. surinamensis as far west as the Maracaibo basin and the presence of E. pearsei and E. panamensis to the west suggests that the northern Andean cordillera, the Sierra del Perijá continues to be a barrier to further dispersal for some species. The Pebas mega-wetland system is however also believed to have been a fluvial system of low salinity ( Boeger and Kritsky 2003; Gross et al. 2015; Gross and Piller 2020) and may have facilitated the dispersal route for extinct turtles by the connectivity between major and minor drainages ( Cadena and Jaramillo 2014). By the Late Miocene to Pliocene, this system had branched extensively to form the drainage systems of the present-day Magdalena, Maracaibo, Orinoco, and Amazonas rivers ( Hoorn et al. 2010). Between 10 and 7 Mya, the Acre system was a series of fluvial connections from the Pebas lake to the Amazon River northeast to the Guianas and may have facilitated dispersal events towards the Amazon ( Hoorn et al. 2010; Albert et al. 2018). More recent evidence suggests that the Pebas system gradually dried out at about 10.5 Mya ( Jaramillo et al. 2017) and after the draining of the wetlands (Late Miocene), diversification in western Amazonia must have been particularly rapid, as the diversity of this area greatly outnumbers the diversity in the cratonic areas. The presence of the Amazon River still today suggests connecting corridors through fluvial systems across the Amazon. It is, therefore, reasonable to assume that the availability of savanna after the Pebas dried out and branching of rivers towards the Amazon River tributaries opened a route of dispersion towards the east.

The colonization routes and events of the Elachistocleis clades present today remain partially tentative as key species are missing from the analyses that could elucidate alternative scenarios. The timing of both clades corresponds well with the transcontinental Amazon River that was formed over a period of about 4.9–5.6 million years, via several river capture events ( Albert et al. 2018) and likely facilitated the dispersal towards the west in the Late Miocene. Our analyses suggest the likely split of E. helianneae + E. nigrogularis from the Amazon Basin region towards a northward expansion to the Guianas about 6 Mya (4.4–8.0, 95% HPD) and a southward expansion of E. bicolor + E. sp. (from Bolivia) towards Brazil at 4.8 Mya (2.8–6.8, 95% HPD). The northern populations (i.e., Guyana) may have originated following the Branco-Essequibo drainage towards the Guianas from northern Amazonas ( Albert et al. 2018).

The phylogeography of the second clade is more intricate and suggests two likely dispersal events. The basal position of E. muiraquitan suggests a western Amazon origin at circa 4.3 Mya (2.9–6.7, 95% HPD) with a northern expansion consisting of species from Panama and Colombia (e.g., E. pearsei ) following the closure of the isthmus of Panama circa 2.5 Mya. In accordance with this timing is the formation of the isthmus sensu stricto, dating to approximately 2.8 Mya (O’ Dea et al. 2016), coinciding with the Great American Biotic Interchange ( Stehli and Webb 1985) over dry land. The divergence of the Colombian and Panamanian species in our analyses agrees with these time estimates. A likely northern migration circa 2.9 Mya (2–3.9, 95% HPD) through the hydrological connections flowing towards the Caribbeandraining Andean foreland, from Los Llanos to Amacuro ( Albert et al. 2018), leading towards the Guianas to what today is the E. surinamensis clade. The relationship of E. piauiensis + E. cesarii can be accounted for either by a southern migration from the Guianas (scenario A, Fig. 3 ) or by an eastern dispersal following the Amazon Basin followed by a coastal southern route (Scenario B, Fig. 3 ) at approximately 2.5 Mya (1.7–3.4, 95% HPD). Molecular sampling of E. carvalhoi and E. bumbameuboi from northern Brazil and E. magnus and E. matogrosso in southern Brazil, proximal to Bolivia, will elucidate important information to ascertain dispersal routes ( Fig. 3 ).

Figures

Fig. 3 MCC discrete coalescent tree of 12S rDNA, 16S rDNA, COI, RAG-1, and TYR sequences. Node circles in red represent posterior probabilities (>0.95) and black nodes (<0.95) and their sizes indicate lower support. Blue bars by nodes denote 95% highest posterior density ranges. The map depicted at the lower left represents the marine incursions in northwestern South America (in dark blue) and the PEBAS wetland lake (light blue) and the red arrows point to likely dispersal routes. The drawing of water in the tree depicts the timing of marine incursions in the Llanos Basin and in the Amazonas/Solimões Basin.