Fabian Herder

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

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 flocks spectacular diversity. To our knowledge, this is the first empirical evidence for massive reticulate evolution within a complex animal radiation.

Environment-contingent sexual selection in a colour polymorphic fish

Sexual selection could be a driving force in the maintenance of intraspecific variation, but supporting observations from nature are limited. Here, we test the hypothesis that spatial heterogeneity of the visual environment can influence sexual selection on colourful male secondary traits such that selective advantage is environment contingent. Using a small fish endemic to Sulawesi, Indonesia (Telmatherina sarasinorum) that has five male colour morphs varying in frequency between two visually distinct mating habitats, we used direct behavioural observations to test the environment-contingent selection hypothesis. These observations were combined with measurements of the visual environment, fish coloration and the sensitivity of visual photopigments to determine whether differential morph conspicuousness was associated with reproductive success across habitats. We found that blue and yellow males are most conspicuous in different habitats, where they also have the highest reproductive fitness. A less conspicuous grey morph also gained high reproductive success in both habitats, raising the possibility that alternative behaviours may also contribute to reproductive success. In a comprehensive analysis, conspicuousness was strongly correlated with reproductive success across morphs and environments. Our results suggest an important role for spatially heterogeneous environments in the maintenance of male colour polymorphism.

ADAPTIVE SYMPATRIC SPECIATION OF POLYCHROMATIC “ROUNDFIN” SAILFIN SILVERSIDE FISH IN LAKE MATANO (SULAWESI)

Abstract The significance of sympatric speciation is one of the most controversial topics in evolutionary biology. Theory suggests that different factors can lead to speciation in full geographical contact, including selection and nonrandom mating. Strict criteria have been established for assessing sympatric speciation, which have been met in only a very few cases. Here, we investigate differentiation among sympatric morphospecies and color morphs of “roundfin” sailfin silversides (Telmatherinidae), small freshwater fish endemic to ancient Lake Matano in Central Sulawesi (Indonesia). Morphospecies are distinct according to body shape (geometric morphometrics), population structure (population-level amplified fragment length polymorphism [AFLP] markers), ecology, and mating behavior (habitat transects, stomach contents). Explorative genome scans based on AFLPs indicate that divergent selection affects only 1.3–4.2% of the analyzed loci, suggesting an early stage of speciation. Transect data demonstrate strong assortative mating and adaptive niche differentiation. However, we find no restrictions in gene flow among the conspicuous male color morphs. In summary, our data are consistent with a sympatric mode of divergence among three morphospecies under conditions effectively ruling out allopatric scenarios. Substantial, but incomplete, reproductive isolation suggests an early stage of speciation, most likely due to ecological selection pressure.

Gene flow at the margin of Lake Matano’s adaptive sailfin silverside radiation: Telmatherinidae of River Petea in Sulawesi

Classical speciation concepts focus almost exclusively on the evolution of strict reproductive isolation as a prerequisite for speciation. However, there is a growing body of evidence indicating that speciation is possible despite or even triggered by gene flow among populations or species. Previous findings indicate that introgressive hybridization is a dominant phenomenon in the adaptive radiation of sailfin silversides (Telmatherinidae) endemic to Lake Matano (Sulawesi). In this study, we investigate patterns of genotypic and phenotypic variation of “sharpfin” sailfin silversides in the outlet area of L. Matano and six locations along River Petea, which is the only connection between L. Matano and other lakes and streams of the Malili Lakes system. Fieldwork revealed no hints for a previously cited major waterfall in River Petea, which was thought to separate L. Matano’s sailfin silverside radiation from the diversity of the downstream lake drainages. Likewise, genomic (AFLP) and morphometric data suggest high levels of gene flow between upper and lower stretches of this river, as well as between riverine Petea and lacustrine Matano populations. Increasing levels of genotypic and phenotypic dissimilarity are correlated with distance over a remarkably short geographic range.

Phenotypic traits meet patterns of resource use in the radiation of “sharpfin” sailfin silverside fish in Lake Matano

Disruptive natural selection on traits related to resource exploitation may lead to differential adaptation and finally to speciation. Trait utility, the performance of traits in terms of fitness, is a central criterion for the recognition of adaptive radiation. Utility of morphological structures involved in foraging can be detected by relating their variation to individual resource use. Here, we test for trophic adaptations in the radiation of “sharpfin” sailfin silversides (Atheriniformes: Telmatherinidae), endemic to ancient graben-lake Matano in central Sulawesi (Indonesia). This small species-flock is characterized by high phenotypic diversity, including traits most likely related to feeding ecology. Previous analyses suggest that species boundaries are porous, indicating very recent or possibly ongoing processes of species flock formation. To test for adaptation to resource use in this radiation, we compared morphological traits among trophic groups of individuals as identified by stomach content analyses. We analyzed variation in candidate structures or structural complexes commonly recognized as indicative of trophic adaptation in fish radiations, including shapes of body, oral and pharyngeal jaws, gill rakers and body size. We found fine-scaled morphological differentiation according to feeding habits, covering all traits analyzed. Fish-, shrimp- and egg-feeders were most distinct, with major axes of morphological variation fitting patterns of adaptation reported from other lacustrine fish radiations. Thus, the present results are consistent with fine-scaled morphological adaptation to resource use, supporting the adaptive character of the sharpfin sailfin silverside radiation.

Beyond Sympatric Speciation: Radiation of Sailfin Silverside Fishes in the Malili Lakes (Sulawesi)

Adaptive radiations of plants and animals play an important role as model systems in speciation research. Rapid emergence of biological diversity provides opportunities to study adaptive and non-adaptive factors leading to speciation, including the role of spatial factors and ecological, behavioral and genetic mechanisms potentially driving speciation processes. The radiation of sailfin silversides (Atheriniformes: Telmatherinidae) endemic to “Wallace’s Dreamponds”, i.e., the Malili Lakes in Central Sulawesi (Indonesia), allows for testing hypotheses of speciation processes under different geographic settings. Compared with other well-known freshwater fish radiations, the Telmatherinid system is of intermediate size in terms of both, geographical size and organismic diversity. Phylogenetic analyses provide evidence for multiple clades that were connected secondarily through reticulate evolution, but combined analyses support an ancient monophyletic origin of all Telmatherinidae clades in Lake Matano. The consensus view is that the lake contains two reciprocally monophyletic groups of sailfin silversides, highly diverse “sharpfins” heavily introgressed by stream populations, and less diverse “roundfins” not affected by allochthonous introgression. Genetic, morphological, habitat-utilization, trophic, and mate-choice data demonstrate that the most plausible hypothesis for the origin of roundfins is by sympatric speciation. Substantial but not absolute restrictions in gene flow coupled with morphological and behavioral adaptations to distinct ecological niches support the hypothesis that natural selection coupled with assortative mating drives speciation processes in roundfins. In contrast, discrete male color polymorphisms can be explained by sexual selection, but appear not to be associated with population divergence. In line with evidence for adaptive radiation in sharpfins, natural selection for distinct resources is certainly a major force shaping diversity in this lacustrine radiation. However, the role of divergent sexual selection on divergence of ecologically diverse sharpfins remains to be tested.

Two New Ricefishes of the Genus Oryzias (Atherinomorpha: Beloniformes: Adrianichthyidae) Augment the Endemic Freshwater Fish Fauna of Southeastern Sulawesi, Indonesia

Oryzias asinua and O. wolasi are two new species of ricefishes described from several disjunct inland freshwater habitats in the Indonesian province of Sulawesi Tenggara or southeastern Sulawesi. With O. woworae, the first described endemic ricefish of Sulawesi Tenggara, they comprise a group of small, colorful species characterized by orange to deep red dorsal and ventral margins of the caudal fin and the ventral margin of the caudal peduncle and at least the posterior portion of the base of the anal fin, and a bluish sheen on the body in both sexes that is most pronounced in live adult males. The two new species are distinguished from O. woworae by elongate middle dorsal-fin rays in adult males that reach the posterior extent of the first principal caudal-fin ray and by an orange-colored olfactory epithelium that marks each nasal organ in females. Oryzias asinua is relatively slender compared to O. wolasi and O. woworae: the body is narrow (21–25% SL, with a mean 22.9, in O. asinua versus 23–32% SL, mean 25.3 in O. wolasi and 22–30% SL, mean 26 in O. woworae). Oryzias asinua has fewer procurrent caudal-fin rays in the lower lobe (4–5 versus 5–7 in O. wolasi and 5–6 in O. woworae). Oryzias wolasi is golden in life in both sexes and relatively deep-bodied, reaching 32% SL, and has a deeper caudal peduncle (11–12% SL, mean 11.2, versus 9–11, mean 10, in O. asinua and 8–11, mean 9.2, in O. woworae). Maximum parsimony and Bayesian inference analyses of the mitochondrial cytochrome c oxidase subunit 1 (COI) sequence, the DNA barcode, support our hypothesis that we sequenced representatives of three species. All species are allopatric. Description of O. asinua and O. wolasi brings the number of valid species in the beloniform family Adrianichthyidae to 35, 17 of which are endemic to Sulawesi. The two new species are just the second and third ricefishes described from the province of Sulawesi Tenggara, a neglected region in exploration and discovery of the freshwater fish fauna of the Indonesian islands of Sulawesi. Oryzias asinua dan O. wolasi adalah dua jenis ikan padi yang dideskripsi dari beberapa, habitat air tawar di Provinsi Sulawesi Tenggara, Indonesia. Bersama O. woworae, ikan padi pertama dari Sulawesi Tenggara yang telah dideskripsi, ketiganya merupakan kelompok jenis berukuran kecil, berpola warna menarik, jingga hingga merah tua pada sirip punggung, tepi sirip ekor bagian bawah, tepi bawah batang ekor dan pada sedikit bagian belakang dari pangkal sirip anal, semburat sinar kebiruan terlihat pada tubuh ikan jantan dan betina, yang tampak jelas terlihat pada pada ikan jantan dewasa yang masih hidup. Ke dua spesies baru tersebut dapat dibedakan dari O. woworae dari jari-jari lemah sirip punggung bagian tengah pada ikan jantan dewasa, yang memanjang dan mencapai bagian posterior sirip ekor pertama, juga dari warna jingga pada epithelium olfactory yang menandai setiap organ nasal pada betina. Oryzias asinua tinggi tubuhnya relatif lebih kecil dibandingkan O. wolasi dan O. woworae: tubuhnya pendek (21–25% SL, rata-rata 22.9% pada O. asinua vs 23–32% SL, rata-rata pada O. wolasi dan 22–30% SL, rata-rata 26% pada O. woworae). Oryzias asinua memiliki lebih sedikit jari lemah tambahan pada cuping ekor bagian bawah (4–5 vs 5–7 pada O. wolasi dan 5–6 pada O. woworae). Pada saat masih hidup Oryzias wolasi berwarna keemasan baik pada jantan dan betina, tubuhnya relatif tinggi, mencapai 32% SL, dan batang ekor lebih tinggi (11–12% SL, rata-rata 11.2 vs 9–11, rata-rata 10, pada O. asinua dan 8–11, rata-rata 9.2, pada O. woworae).Maksimum parsimony dan analisa Bayesian inference pada sekuens mitochondrial cytochrome c oxidase subunit 1 (COI) atau sekuens DNA barcode selaras dengan hipotesis kami yang mensekuen sampel dari ketiga spesies tersebut. Ketiga spesies ini bersifat allopatrik. Dengan deskripsi dari O.asinua dan O.wolasi maka spesies valid pada beloniform famili Adrianichthyidae menjadi 35, 17 diantaranya endemik di Sulawesi. Dua spesies baru adalah ikan padi kedua dan ketiga yang dideskripsikan dari Provinsi Sulawesi Tenggara, wilayah yang terabaikan dari eksplorasi dan penemuan fauna ikan air tawar di Sulawesi, salah satu dari kepulauan di Indonesia.

Spectral data reveal unexpected cryptic colour polymorphism in female sailfin silverside fish from ancient Lake Matano

Persistent colour polymorphisms can result from natural and/or sexual selection, and may occur in males, females, or both sexes. Contrary to conspicuous patterns frequently observed in courtship colouration, differences in cryptic colouration are not always perceived by the human sensory system. In sexually dimorphic sailfin silversides fishes, males show conspicuous colour polymorphisms whereas females appear monomorphic and cryptic. We measured the spectral composition of body, fin and peduncle colouration in male and female Telmatherina antoniae ‘small’, a sailfin silverside species endemic to ancient Lake Matano, and found evidence for a colour polymorphism in both sexes. The three colour morphs distinguished by spectral data correspond to those commonly reported for males, and are also present in the visually (to a human eye) cryptic females. Females show hue value patterns similar to those present in males, but differ from males substantially in chroma and brightness. This is, to the best of our knowledge, the first example of a cryptic colour polymorphism in fishes; however, its significance for the mating system remains unknown. The present finding highlights the need for incorporating female spectral data into analyses of colour patterns, and suggests that colour analyses should include cryptic sexes.

Alternative egg-feeding tactics in Telmatherina sarasinorum, a trophic specialist of Lake Matano’s evolving sailfin silversides fish radiation

Feeding specialisation is a typical feature of adaptive animal radiations. Different kinds of feeding specialisations have evolved in the endemic sailfin silversides species flock in Lake Matano (Central Sulawesi, Indonesia), including egg-feeding. The present study focuses on Telmatherina sarasinorum, a sailfin silverside species feeding on the eggs of related Telmatherina antoniae. Stomach content analyses supported T. antoniae eggs to be the dominant food item, independent of daytime. We hypothesized that the egg-feeders use alternative tactics for maximising egg consumption under varying densities of both, spawning T. antoniae pairs and competing conspecific egg-feeders. Focal behavioural observations were applied to describe different feeding tactics and to analyse feeding success and the related costs in terms of competitive interactions. Egg-feeders followed single courting pairs of T. antoniae or, alternatively, they switched between different spawning pairs. Following-behaviour, covering one or more spawning events of the host species, was positively related to enhanced egg consumption. Compared to feeding by switching frequently among different spawning pairs, the following tactic came at the cost of likewise increased competition. Behavioural observations suggest that some males monopolize courting pairs of T. antoniae and gain increased amounts of eggs compared to others avoiding competition by switching among pairs. The present results confirm that egg-feeding is a distinct trophic specialisation in T. sarasinorum and increase the scale of behavioural specialisation in Lake Matano’s evolving Telmatherina radiation.

Rugged adaptive landscapes shape a complex, sympatric radiation.

Strong disruptive ecological selection can initiate speciation, even in the absence of physical isolation of diverging populations. Species evolving under disruptive ecological selection are expected to be ecologically distinct but, at least initially, genetically weakly differentiated. Strong selection and the associated fitness advantages of narrowly adapted individuals, coupled with assortative mating, are predicted to overcome the homogenizing effects of gene flow. Theoretical plausibility is, however, contrasted by limited evidence for the existence of rugged adaptive landscapes in nature. We found evidence for multiple, disruptive ecological selection regimes that have promoted divergence in the sympatric, incipient radiation of ‘sharpfin’ sailfin silverside fishes in ancient Lake Matano (Sulawesi, Indonesia). Various modes of ecological specialization have led to adaptive morphological differences between the species, and differently adapted morphs display significant but incomplete reproductive isolation. Individual fitness and variation in morphological key characters show that disruptive selection shapes a rugged adaptive landscape in this small but complex incipient lake fish radiation.