Dynamic reticulate evolution in a Daphnia multispecies complex

Abstract

Recent genomic data suggest that the role of hybridization in evolution might be more important than previously assumed. Here, we examine species-specific differentiation and signatures of reticulation in a multi-species complex of the crustacean genus Daphnia. We did a combined examination of mtDNA, allozymes and ITS1 (a part of the nuclear ribosomal DNA) in the Daphnia longispina group. We focused on the sequence variation of ITS1 in two unambiguous species (D. galeata, D. cucullata) and two ecotypes hyalina and rosea within the recently revised taxon D. longispina (O.F. Müller). We found two ITS1-types (S, L) and intra-individual and intra-specific polymorphisms. Another ITS1-type (XL) was restricted to the outgroup D. umbra. S was present in all taxa but occurred as only two variants. Surprisingly, D. galeata and D. cucullata, which were well differentiated by mtDNA and allozymes, were virtually indistinguishable with respect to S-ITS1 (S(cg)). The two ecotypes of D. longispina shared the second S-ITS1-variant (S(rh)) and were therefore almost indistinguishable for all types of molecular markers surveyed. The L-type differed between D. galeata and D. longispina samples, but L was absent in D. cucullata. Between hyalina and rosea ecotypes, we found some L-differentiation. Combined data suggest that reticulate evolution enabled the spread of one S-ITS1-variant (S(cg)) beyond species boundaries and that S-introgression was species-specific, despite contemporary hybridization between all species. Our data have implications for phylogenetic as well as phylogeographic surveys. Because of the dynamic impact of gene flow in multi-species complexes, misinterpretations of presumed species-specific data should be considered.

Identifying hybridizing taxa within the Daphnia longispina species complex: a comparison of genetic methods and phenotypic approaches

“…We agree with the conclusions of Gießler & Englbrecht (2009), who warn against using ITS-RFLP for taxon identification. Nevertheless, if properly validated for specific study questions, it may remain a convenient method for genotyping large-sized samples, especially from ethanol-preserved material.…”

“…However, recent studies (Petrusek et al, 2008a;Thielsch et al, 2009) suggest that the lakeinhabiting form D. hyalina, the mostly pond-inhabiting D. rosea, as well as various intermediate morphotypes just represent morphs of the single phenotypically variable biological species D. longispina. This conclusion is supported by the lack of genetic divergence in various molecular markers, such as mitochondrial DNA (Petrusek et al, 2008a), allozymes (Gießler et al, 1999), 13 unlinked microsatellite loci (Thielsch et al, 2009), and nuclear ITS sequences (Gießler & Englbrecht, 2009). Individuals identified as D. longispina from localities sampled in this study included typical D. hyalina-like morphotypes as well as transitional forms closer to D. rosea morphology.…”

“…Evidence of such processes can also be found in other populations of the D. longispina complex. Gießler & Englbrecht (2009) Relative success of the determination is shown as the percentage of individuals determined identically by both phenotype and molecular methods from the total number of determined individuals of that particular taxon. In cases where the total N is \240, the person did not determine all individuals from the data set.…”

“…In such cases, gene pools of the parental species might be partly fused and inconsistencies among the species-specific markers may occur (Harrison, 1990;Arnold, 1992). The importance of this process has been emphasized in some studies Gießler et al, 1999;Gießler & Englbrecht, 2009) which consider the D. longispina species complex as a group of taxa with incomplete reproductive isolation. Thus, species phylogeny could exhibit a reticulate rather than hierarchical pattern of evolution.…”

“…Gene flow among parental species may cause reticulate patterns of evolution which potentially lead to increased levels of genetic and morphological variability in local populations (Schwenk & Spaak, 1997). Although some studies suggest reticulate evolution plays an important role for the D. longispina complex Gießler et al, 1999;Gießler & Englbrecht, 2009), gene pools of parental species seem to remain distinct , and might be well distinguished by various molecular methods (e.g., Thielsch et al, 2009).…”