Age estimates for an adaptive lake fish radiation, its mitochondrial introgression, and an unexpected sister group: Sailfin silversides of the Malili Lakes system in Sulawesi

Abstract

Background: The Malili Lakes system in central Sulawesi (Indonesia) is a hotspot of freshwater biodiversity in the Wallacea, characterized by endemic species flocks like the sailfin silversides (Teleostei: Atherinomorpha: Telmatherinidae) radiation. Phylogenetic reconstructions of these freshwater fishes have previously revealed two Lake Matano Telmatherina lineages (sharpfins and roundfins) forming an ancient monophyletic group, which is however masked by introgressive hybridization of sharpfins with riverine populations. The present study uses mitochondrial data, newly included taxa, and different external calibration points, to estimate the age of speciation and hybridization processes, and to test for phylogeographic relationships between Kalyptatherina from ancient islands off New Guinea, Marosatherina from SW Sulawesi, and the Malili Lakes flock.

Results: Contrary to previous expectations, Kalyptatherina is the closest relative to the Malili Lakes Telmatherinidae, and Marosatherina is the sister to this clade. Palaeogeographic reconstructions of Sulawesi suggest that the closer relationship of the Malili Lakes radiation to Kalyptatherina might be explained by a 'terrane-rafting' scenario, while proto-Marosatherina might have colonized Sulawesi by marine dispersal. The most plausible analysis conducted here implies an age of c. 1.9 My for the onset of divergence between the two major clades endemic to Lake Matano. Diversification within both lineages is apparently considerably more recent (c. 1.0 My); stream haplotypes present in the sharpfins are of even more recent origin (c. 0.4 My).

Conclusions: Sulawesi's Telmatherinidae have most likely originated in the Sahul Shelf area, have possibly reached the island by both, marine dispersal and island/terrane-rafting, and have colonized the Malili Lakes system from rivers. Estimates for the split between the epibenthic sharpfins and the predominantly pelagic to benthopelagic roundfins in Lake Matano widely coincide with geological age estimates of this rift lake. Diversification within both clades clearly predates hybridization events with stream populations. For Lake Matano, these results support a scenario of initial benthic-pelagic divergence after colonization of the lake by riverine populations, followed by rapid radiation within both clades within the last 1 My. Secondary hybridization of stream populations with the sharpfins occurred more recently, and has thus most likely not contributed to the initial divergence of this benthic species flock.

Figure 1

BEAST MCC tree showing general melanotaeniid and telmatherinid relationships for the concatenated dataset. Topology derived from analysis [D]. Numbers on branches denote RAxML bootstrap values, MrBayes posterior probabilities and BEAST posterior probabilities (from top to bottom); numbers on nodes correspond to node numbers given in Table  2, i.e., divergence time estimates across all four analyses performed. Nodes 1 and 9 were used as indirect and geological calibration points, respectively (see Methods for details). Abbreviations used for sailfin silversides: MAH = Lake Mahalona; MAT = Lake Matano; TOW = Lake Towuti. See text and Figure  3 for details on the Lake Matano telmatherinid radiation. Map shows current distribution of Kalyptatherina, Marosatherina, and the Malili Lakes telmatherinds.

Figure 2

Phylogenetic hypotheses showing the systematic position of Telmatherinidae and relatives among different studies. (A)[39], (B)[22], (C)[32], (D)[24], (E)[40], (F) Present study. Telmatherinid representatives are highlighted in grey. See text for details.

Figure 3

Relaxed-clock divergence times distribution among analyses for the Lake Matano telmatherinid radiation. Bars denote 95% credibility intervals, dots represent mean ages for MRCAs of the respective clades. See Methods and Table  2 for details.

Figure 4

Palaeogeographic maps of SE Asia, with particular focus on West Sulawesi and the Sula Spur. Modified from [51], with permission (see text for details).