Evolutionary Divergence and Radula Diversification in Two Ecomorphs from an Adaptive Radiation of Freshwater Snails.

(1) Background: Adaptive diversification of complex traits plays a pivotal role in the evolution of organismal diversity. In the freshwater snail genus Tylomelania, adaptive radiations were likely promoted by trophic specialization via diversification of their key foraging organ, the radula. (2) Methods: To investigate the molecular basis of radula diversification and its contribution to lineage divergence, we used tissue-specific transcriptomes of two sympatric Tylomelania sarasinorum ecomorphs. (3) Results: We show that ecomorphs are genetically divergent lineages with habitat-correlated abundances. Sequence divergence and the proportion of highly differentially expressed genes are significantly higher between radula transcriptomes compared to the mantle and foot. However, the same is not true when all differentially expressed genes or only non-synonymous SNPs are considered. Finally, putative homologs of some candidate genes for radula diversification (hh, arx, gbb) were also found to contribute to trophic specialization in cichlids and Darwin's finches. (4) Conclusions: Our results are in line with diversifying selection on the radula driving Tylomelania ecomorph divergence and indicate that some molecular pathways may be especially prone to adaptive diversification, even across phylogenetically distant animal groups.

Sexual dimorphism in an adaptive radiation: Does intersexual niche differentiation result in ecological character displacement?

Evolutionary radiations are one plausible explanation for the rich biodiversity on Earth. Adaptive radiations are the most studied form of evolutionary radiations, and ecological opportunity has been identified as one factor permitting them. Competition among individuals is supposedly highest in populations of conspecifics. Divergent modes of resource use might minimize trophic overlap, and thus intersexual competition, resulting in ecological character displacement between sexes. However, the role of intersexual differentiation in speciation processes is insufficiently studied. The few studies available suggest that intersexual niche differentiation exists in adaptive radiations, but their role within the radiation, and the extent of differentiation within the organism itself, remains largely unexplored. Here, we test the hypothesis that multiple morphological structures are affected by intersexual niche differentiation in "roundfin" Telmatherina, the first case where intersexual niche differentiation was demonstrated in an adaptive fish radiation. We show that sexes of two of the three morphospecies differ in several structural components of the head, all of these are likely adaptive. Sexual dimorphism is linked to the respective morphospecies-specific ecology and affects several axes of variation. Trait variation translates into different feeding modes, processing types, and habitat usages that add to interspecific variation in all three morphospecies. Intrasexual selection, that is, male-male competition, may contribute to variation in some of the traits, but appears unlikely in internal structures, which are invisible to other individuals. We conclude that intersexual variation adds to the adaptive diversity of roundfins and might play a key role in minimizing intersexual competition in emerging radiations.

Do we need the third dimension? Quantifying the effect of the z-axis in 3D geometric morphometrics based on sailfin silversides (Telmatherinidae).

This study investigated the impact of the third dimension in geometric morphometrics (GM) using sailfin silversides (Telmatherinidae) from the Malili Lakes of Sulawesi (Indonesia). The three morphospecies of the monophyletic "roundfin" radiation are laterally compressed and vary in shape traits. The results of 2D and 3D GM were compared and quantified to discuss the advantages and disadvantages of both methods for closely related species and their sexes. This approach focused on the head because it is far more complex and three-dimensionally structured than the trunk or the caudal region. The results revealed no significant benefit concerning repeatability and measurement error in 3D GM compared to 2D GM. The z-axis contributed substantially to the variance of the 3D data set but was irrelevant for discrimination of species and sexes in the approach. Limited gain in information was contrasted by substantially higher effort for 3D compared to the 2D analyses. The study concluded that 2D GM is the more efficient shape analysis approach for discriminating roundfins. Broader studies are needed to test which of the two methods is more efficient in distinguishing laterally compressed fishes in general. For future studies, due to the high investment required, this study recommends carefully evaluating the necessity of 3D GM. If in doubt, this study suggests testing for congruence between 2D and 3D GM with a subsample and consequently applying 2D GM in the case of high congruence.

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.

The complete mitochondrial genome of the viviparous freshwater snail Tylomelania sarasinorum (Caenogastropoda: Cerithioidea).

Here, we present the first complete mitochondrial genome within the gastropod family Pachychilidae, using the viviparous freshwater snail Tylomelania sarasinorum. This species is a representative member of the lacustrine Tylomelania radiations of the Malili-Lakes-System (Sulawesi, Indonesia). The mitochondrial genome was 16,632 bp long and contained 13 protein-coding genes, 2 rRNA genes and 22 tRNA genes. A pronounced A + T bias was observed with an overall base composition of 29.5% A, 35.7% T, 18.3% G and 16.6% C. Tylomelania sarasinorum exhibited a novel mitochondrial gene arrangement, differing from all Caenogastropoda mitochondrial genomes published to date.

Adaptive sympatric speciation of polychromatic "roundfin" sailfin silverside fish in Lake Matano (Sulawesi).

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.

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