Adaptive radiation and hybridization in Wallace's Dreamponds: evidence from sailfin silversides in the Malili Lakes of Sulawesi

Abstract

Adaptive radiations are extremely useful to understand factors driving speciation. A challenge in speciation research is to distinguish forces creating novelties and those relevant to divergence and adaptation. Recently, hybridization has regained major interest as a potential force leading to functional novelty and to the genesis of new species. Here, we show that introgressive hybridization is a prominent phenomenon in the radiation of sailfin silversides (Teleostei: Atheriniformes: Telmatherinidae) inhabiting the ancient Malili Lakes of Sulawesi, correlating conspicuously with patterns of increased diversity. We found the most diverse lacustrine species-group of the radiation to be heavily introgressed by genotypes originating from streams of the lake system, an effect that has masked the primary phylogenetic pattern of the flock. We conclude that hybridization could have acted as a key factor in the generation of the flock's spectacular diversity. To our knowledge, this is the first empirical evidence for massive reticulate evolution within a complex animal radiation.

Figure 1

The Malili Lakes system and its endemic sailfin silversides. L. Matano is a very deep (590 m) graben-lake, drained by the steep R. Petea to L. Mahalona, from where the flow continues to L. Towuti. L. Towuti is drained to the sea. Lake Lontoa is connected by a stream to L. Towuti; no telmatherinids were found in L. Masapi. Fish inside the lakes represent the major groups of lake phenotypes. Sampling locations of stream telmatherinids are indicated as dots, with numbers referring to location names specified in electronic supplementary material Table 2. Map by von Rintelen & Zitzler, modified with permission.

Figure 2

Phylogenies of Malili Lakes telmatherinids. (a) Bayesian tree of mitochondrial haplotypes, rooted with Marosatherina (SW-Sulawesi). The numbers above branches refer to Bayesian posterior probabilities of the major nodes. Bootstrap and jackknife values (more than 50%; upper and lower values, respectively) are shown below branches. (b) Distance-based phylogenetic AFLP network. Compatible collections of splits are displayed tree-like, conflicting signal as boxes. Strongest conflict is indicated for the ‘stream-clade’ and for L. Matano's ‘sharpfins’. Substantial conflict is also present in the centre of the network, suggesting strong reticulate patterns within the whole species-flock. Enlarged figures and specimens are provided in electronic supplementary material figures 1 and 2.

Figure 3

Test for signal of hybridization. Relative bootstrap support (2000 replicates) for the clade of ‘stream phenotypes’ when removing experimentally selected samples. Bars display 97 out of 100 random removals (three experimental topologies did not support stream phenotypes as monophyletic). Black sections illustrate complete removal of each of the six remaining clades, corrected to standardized number of exclusions (19) by adding randomly selected samples. Asterisk marks the stream phenotypes support value given the complete dataset. The arrow denotes the far outside value (99%) resulting from the exclusion of all sharpfins.

Figure 4

Principal component scatterplot (axes 1 and 2) based on geometric morphometry. Lines surround areas in morphospace occupied by the endemic radiations of Lake Matano's sharpfins and roundfins and stream populations inhabiting surrounding water bodies. Both sympatric lake clades largely differ from each other and from the allopatric stream populations. Morphospace occupied by sharpfins is conspicuously higher than by roundfins or stream phenotypes.