Evidence for Sympatric Speciation in a Wallacean Ancient Lake
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ORIGINAL ARTICLE doi:10.1111/evo.13821 Evidence for sympatric speciation in a Wallacean ancient lake Nobu Sutra,1 Junko Kusumi,2 Javier Montenegro,1 Hirozumi Kobayashi,1 Shingo Fujimoto,3 Kawilarang W. A. Masengi,4 Atsushi J. Nagano,5 Atsushi Toyoda,6 Masatoshi Matsunami,3 Ryosuke Kimura,3 and Kazunori Yamahira1,7 1Tropical Biosphere Research Center, University of the Ryukyus, Okinawa 903-0213, Japan 2Faculty of Social and Cultural Studies, Kyushu University, Fukuoka 819-0395, Japan 3Graduate School of Medicine, University of the Ryukyus, Okinawa 903-0125, Japan 4Faculty of Fisheries and Marine Science, Sam Ratulangi University, Manado 95115, Indonesia 5Faculty of Agriculture, Ryukoku University, Otsu 520-2194, Japan 6Comparative Genomics Laboratory, National Institute of Genetics, Mishima 411-8540, Japan 7E-mail: [email protected] Received March 4, 2019 Accepted August 3, 2019 Sympatric speciation has been demonstrated in few empirical case studies, despite intense searches, because of difficulties in testing the criteria for this mode of speciation. Here, we report a possible case of sympatric speciation in ricefishes of the genus Oryzias on Sulawesi, an island of Wallacea. Three species of Oryzias are known to be endemic to Lake Poso, an ancient tectonic lake in central Sulawesi. Phylogenetic analyses using RAD-seq-derived single nucleotide polymorphisms (SNPs) revealed that these species are monophyletic. We also found that the three species are morphologically distinguishable and clearly separated by population-structure analyses based on the SNPs, suggesting that they are reproductively isolated from each other. A mitochon- drial DNA chronogram suggested that their speciation events occurred after formation of the tectonic lake, and existence of a historical allopatric phase was not supported by coalescent-based demographic inference. Demographic inference also suggested introgressive hybridization from an outgroup population. However, differential admixture among the sympatric species was not supported by any statistical tests. These results all concur with criteria necessary to demonstrate sympatric speciation. Ricefishes in this Wallacean lake provide a promising new model system for the study of sympatric speciation. KEY WORDS: Allopatric phase, demography, introgressive hybridization, Oryzias, reproductive isolation, Sulawesi. Sympatric speciation, the process through which new species see Bolnick and Fitzpatrick 2007 for review). Some consider that evolve from a single ancestral species in the absence of geograph- this is not due to its rarity, but because of the difficulty of em- ical barriers, has been a central subject in evolutionary biology pirically demonstrating this mode of speciation (e.g., Bird et al. since Darwin’s “principle of divergence” (e.g., Mayr 1992; Turelli 2012). et al. 2001). Although subsequent theories contend that sympatric It is proposed that four criteria need to be satisfied to demon- speciation is possible under certain conditions (e.g., Dieckmann strate sympatric speciation (Coyne and Orr 2004): (1) sympatric and Doebeli 1999; Higashi et al. 1999; Kondrashov and Kon- contemporary distributions, (2) genetically based substantial re- drashov 1999; see Bolnick and Fitzpatrick 2007 for review), only productive isolation, (3) phylogenetic sister relationships, and (4) a few empirical case studies demonstrating this mode of specia- no historic phase of geographic isolation. However, inferences tion are known (e.g., Schliewen et al. 1994; Sorenson et al. 2003; of the phylogenetic sister relationship (criterion 3) may be mis- Barluenga et al. 2006; Savolainen et al. 2006; Herder et al. 2008; guided when only data for mitochondrial DNA (mtDNA) and/or C 2019 The Author(s). Evolution C 2019 The Society for the Study of Evolution. 1 Evolution N. SUTRA ET AL. a few nuclear genes are used (Maddison 1997; Nichols 2001). and the resultant lake formations are the primary factors promot- Also, inferences based only on a small number of genes might not ing diversification of these lacustrine lineages and shape their be sufficient to capture genetically based reproductive isolation current distributions (Mokodongan and Yamahira 2015a). How- (criterion 2) when lineage-sorting is incomplete (e.g., Kutschera ever, it remains unclear in most cases how species within each et al. 2014; Zhou et al. 2017; Marques et al. 2019). The absence lineage have diverged. of an allopatric phase in the past (criterion 4) is also generally Three species of Oryzias, namely Oryzias nebulosus Parenti difficult to demonstrate because it requires concrete information &Soeroto,Oryzias orthognathus Kottelat, and Oryzias nigrimas on the geological history of the relevant region and/or on the Kottelat, are known to be endemic to Lake Poso, an ancient tec- demographic history of the species themselves. Therefore, very tonic lake in central Sulawesi (Kottelat 1990; Parenti and Soeroto few case studies have met these criteria despite intensive searches 2004). The age of this lake is estimated to be 1–2 million years (Coyne and Orr 2004; Bolnick and Fitzpatrick 2007). (von Rintelen et al.2004; von Rintelen and Glaubrecht 2006; see In addition to these standard criteria, the role of introgres- Fig. S1 for a bathymetry map of the lake). The mtDNA phyloge- sive hybridization due to secondary gene flow from outgroup nies suggested that these three species are monophyletic (Fig. 1) populations in the process of sympatric speciation is recently at- (cf. Mokodongan and Yamahira 2015a,b). Their complete en- tracting more attention because sympatric divergence could be demism and monophyly imply that they diverged in sympatry aided by secondary gene flow (e.g., Martin et al. 2015; Kautt within the lake. Because the three species could be collected et al. 2016; Meier et al. 2017; Foote 2018). For example, genetic at the same time from a single site on the lake (see Materials variants supplied by secondary gene flow may be absorbed into and Methods section), the first criterion of sympatric distribu- the gene pool, leading to formation of a hybrid swarm and in- tions (criterion 1) is satisfied. However, the other three criteria creased genetic variation within the population, which may be have not been examined rigorously. Especially, no study has yet sufficient to trigger later sympatric divergence (Richards et al. demonstrated genetically based reproductive isolation among the 2019). In contrast, population divergence might occur without three species (criterion 2) or the absence of a historic phase of reaching panmixia, which will be the case when reproductive geographic isolation during their divergence (criterion 4). isolation between colonists and occupants is strengthened by re- Moreover, possible introgressive hybridization from an out- inforcement and/or ecological character displacement (Seehausen group population in this system also requires examination. The 2004; Pfennig and Pfennig 2012). In these scenarios, genetic vari- three Poso species are sisters to another Oryzias species, Oryzias ants from outgroups will be differentially sorted into subsequent soerotoi Mokodongan, Tanaka & Yamahira, which inhabits Lake populations. On the other hand, secondary gene flow may trigger Tiu, located 65 km east of Lake Poso (Fig. 1) (Mokodongan et al. initial sympatric divergence (Richards et al. 2019), where differ- 2014). The sister relationship between the Poso and Tiu species ential admixture will not occur. In all above cases, an initial level suggests that these two lakes were once a single lake or lake of divergence between species is triggered by allopatric diver- system, or that colonization occurred from one lake to the other. gence; this is therefore called “gene flow induced sympatric diver- The fact that the river system connected with Lake Tiu comes gence” as opposed to “hard sympatric speciation” (Richards et al. very close to Lake Poso (about 5 km at the closest point; Fig. 1) 2019). supports these views. Either way, the scenario that speciation in Here, we report a possible case of sympatric speciation in Lake Poso was aided by introgressive hybridization as a result of ricefishes (Adrianichthyidae) of the genus Oryzias on Sulawesi subsequent gene flow from Lake Tiu needs to be tested. Island, eastern Indonesia. Sulawesi is the largest island of Wal- In this study, we present evidence consistent with the hypoth- lacea, a group of islands located between the Sunda Shelf and the esis that the three Oryzias species in Lake Poso diverged within continental shelf of Australia. Previous molecular phylogenetic the lake. First, we show that these three sympatric species are analyses revealed that these Sulawesi adrianichthyids are mono- valid morphological and biological species that are reproductively phyletic (Takehana et al. 2005; Herder et al. 2012; Mokodongan isolated from each other using morphologies and population- and Yamahira 2015a,b; Mandagi et al. 2018), suggesting that they genomic analysis of genome-wide single-nucleotide polymor- diverged within the island from a single common ancestor. It has phisms (SNPs). Second, we confirm that the three species are been demonstrated that the divergence of major clades from this monophyletic and sisters to the outgroup through phylogenetic common ancestor largely reflects the complex geological history analysis of the genome-wide SNP data. Third, we demonstrate of this island (Mokodongan and Yamahira 2015a). Especially, the absence of a historical allopatric phase by approaches