Adaptive Radiation and Hybridization in Wallace's Dreamponds: Evidence from Sailfin Silversides in the Malili Lakes of Sulawes

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Adaptive Radiation and Hybridization in Wallace's Dreamponds: Evidence from Sailfin Silversides in the Malili Lakes of Sulawes Proc. R. Soc. B (2006) 273, 2209–2217 doi:10.1098/rspb.2006.3558 Published online 22 June 2006 Adaptive radiation and hybridization in Wallace’s Dreamponds: evidence from sailfin silversides in the Malili Lakes of Sulawesi Fabian Herder1,4,*, Arne W. Nolte2, Jobst Pfaender1, Julia Schwarzer1, Renny K. Hadiaty3 and Ulrich K. Schliewen4 1Sektion Ichthyologie, Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, 53113 Bonn, Germany 2Institute for Genetics, University of Cologne, Weyertal 121, 50931 Ko¨ln, Germany 3Ichthyology Laboratory, Division of Zoology, Research Center for Biology, Indonesian Institute of Sciences (LIPI), Jl. Raya Bogor Km 46, Cibinong 16911, Indonesia 4Department of Ichthyology, Bavarian State Collection of Zoology (ZSM), Mu¨nchhausenstr 21, 81247 Mu¨nchen, Germany 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. Keywords: hybridization; introgression; adaptive radiation; Malili Lakes; Telmatherinidae; amplified fragment length polymorphism 1. INTRODUCTION processes, it is only recently that hybridization has been Introgressive hybridization can play a significant role in proposed as a major explanatory factor for the generation evolution by creating novel gene combinations, which in of diversity (Seehausen 2004). Indeed, recent molecular turn may create key innovations leading to expansions of phylogenetic evidence shows that introgression and hybrid niche, habitat or range (Gilbert 2003; Rieseberg et al. 2003; speciation has occurred within species flocks (Barrier et al. Grant et al. 2004). Although it remains debatable whether 1999; Ru¨ber et al. 2001; Salzburger et al.2002; Shaw 2002; introgressive hybridization and hybrid speciation contrib- Smith et al.2003; Schliewen & Klee 2004; Sullivan et al. ute significantly to the generation of global species diversity 2004; Joyce et al. 2005). However, unequivocal evidence (Arnold 1997; Dowling & Secor 1997; Barton 2001), most for large scale hybridization events that are related to the authors agree that overall fitness of introgressed popu- evolution of megadiversity is still lacking. lations may reach its highest levels in novel habitats, when Reasons for the deficiency in knowledge concerning the selection intensity against introgressed alleles is low and the evolutionary role of hybridization lie partially in methodo- evolution along new evolutionary trajectories is facilitated logical problems (Seehausen 2004). However, the ampli- (Grant et al. 2004; Nolte et al. 2005). fied fragment length polymorphism (AFLP) technique (Vos Adaptive radiations are prime examples for the et al. 1995) constitutes a powerful tool to investigate ‘explosive’ genesis of biodiversity in novel habitats such phylogenetic relationships within species flocks (Albertson as newly formed lakes. Some of these harbour species et al. 1999; Allender et al. 2003; Schliewen & Klee 2004; flocks containing hundreds of endemic species, e.g. the Sullivan et al.2004) with the advantage to provide cichlids of ‘Darwin’s Dreamponds’ (Goldschmidt 1998), numerous unlinked nuclear loci. These can be used to test i.e. the East African Great Lakes (Turner et al.2001; hypotheses of hybridization by screening for homoplastic Kocher 2004). Although these systems have served for effects in phylogenetic trees (Seehausen 2004;see§2d ). A second major problem is the need to study ideally all decades as natural laboratories for the study of speciation potential partners of the hybridization scenario in order to quantify the contribution of introgressive hybridization to * Author for correspondence ([email protected]). speciation processes. To overcome the problem of com- plexity, radiations with lower species richness and less The electronic supplementary material is available at http://dx.doi. org/10.1098/rspb.2006.3558 or via http://www.journals.royalsoc.ac. spatial complexity (McKaye et al. 2002; Schliewen & Klee uk. 2004) or single pairs of sympatric species (Pigeon et al. Received 23 December 2005 2209 q 2006 The Royal Society Accepted 21 March 2006 2210 F. Herder and others Radiation and hybridization 3 2 4 stream Nuha 1 stream West Lake Matano 6 5 7 River Petea 100 km Lake Mahalona Lake Lontoa 8 River Tominanga 13 River Larona 12 9 Lake Towuti depth (m) –100 –150 Lake Masapi 10 –200 –300 –400 11 –500 –550 10 km 14 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. 1997; Lu & Bernatchez 1999; Turgeon et al. 1999; sharpfins than in the predominantly pelagic roundfins McKinnon & Rundle 2002) have been developed as (Herder et al. in press; supplementary table 1). In rivers models. However, to understand the mechanisms shaping and streams of the Malili Lakes drainage system, as well as whole radiations, model systems should be larger than a in several isolated neighbouring watersheds, morpho- single species pair but small enough to be covered almost logically more or less distinct stream populations completely. Recent molecular phylogenetic evidence (Telmatherina cf. bonti ) were recently discovered (figure 1; based on freshwater gastropods (von Rintelen et al. supplementary table 2). 2004) and fishes (Roy et al. 2004) suggest strongly that Here, we use multilocus AFLP marker and mito- the organismic diversity of the Malili Lakes of Central chondrial haplotypes to test for phylogenetic signals of Sulawesi (Indonesia) may represent such a system. This ancient or ongoing introgressive hybridization during ancient lake system (Brooks 1950) consists of the three species flock formation. Tests based on the multilocus main lakes, Matano, Towuti and Mahalona, and two dataset are applied to demonstrate that hybridization is a smaller lakes, Lontoa and Masapi (figure 1). They harbour common phenomenon in the radiation of sailfin silver- an endemic species flock of sailfin silversides (Teleostei: sides. There is a conspicuous correlation of the high Atheriniformes: Telmatherinidae; see figures 1 and 2), morphological diversity and pronounced patterns of hybridization in the adaptive radiation of L. Matano’s which exhibit a conspicuous chromatic polymorphism in sharpfins. We discuss findings in the context of hybrid male coloration in several species consisting of ‘yellow’ speciation in species flocks. and ‘blue’ colour components; they are endemic either to Lakes Towuti and Mahalona or to isolated L. Matano alone (Kottelat 1990, 1991; Herder et al. in press). Their 2. MATERIAL AND METHODS diversity comprises the genera Paratherina, Tominanga and (a) Study system Telmatherina. Lake Matano’s Telmatherina can be assigned The Malili Lakes system is located in the central highland of according to shape of their second dorsal and anal fins to Sulawesi. Its main lakes have a size of 24–561 km2, are ‘roundfins’ and ‘sharpfins’ (Kottelat 1991), with consider- characterized by crystal clear water and are interconnected by ably higher diversity in the predominantly benthic rivers or streams, allowing for contact among sailfin silverside Proc. R. Soc. B (2006) Proc. R. Soc. B (a) Marosatherina ladigesi Lakes Towuti/Mahalona/Lontoa Lake Matano Surrounding streams 0.80 74 73 Paratherina (Towuti/Mahalona) Telmatherina roundfins (Matano) Telmatherina cf. bonti (streams) (2006) 0.79 69 77 Telmatherina celebensis (Towuti/Mahalona/Lontoa) Telmatherina sharpfins (Matano) Telmatherina cf. bonti West (West-stream) 1.00 99 99 Tominanga (Towuti/Mahalona) Bootstrap-support (2000 replicates) 0.66 -- -- 100 (b) 100 100 1.00 98 96 91 99 1.00 98 Radiation and hybridization 99 98 1.00 100 100 1.00 56 82 92 1.00 1 change 84 78 1.0 0.68 -- -- 0.89 87 80 0.88 F. Herder and others 2211 93 92 1.00 99 98 0.96 55 -- 10.0 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
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