Mitochondrial Capture Misleads about Ecological Speciation in the Daphnia pulex Complex

The North American ecological species Daphnia pulicaria and Daphnia pulex are thought to have diverged from a common ancestor by adaptation to sympatric but ecologically distinct lake and pond habitats respectively. Based on mtDNA relationships, European D . pulicaria is considered a different species only distantly related to its North American counterpart, but both species share a lactate dehydrogenase (Ldh) allele F supposedly involved in lake adaptation in North America, and the same allele is also carried by the related Holarctic Daphnia tenebrosa . The correct inference of the species’ ancestral relationships is therefore critical for understanding the origin of their adaptive divergence. Our species tree inferred from unlinked nuclear loci for D . pulicaria and D . pulex resolved the European and North American D . pulicaria as sister clades, and we argue that the discordant mtDNA gene tree is best explained by capture of D . pulex mtDNA by D . pulicaria in North America. The Ldh gene tree shows that F-class alleles in D . pulicaria and D . tenebrosa are due to common descent (as opposed to introgression), with D . tenebrosa alleles paraphyletic with respect to D . pulicaria alleles. That D . tenebrosa still segregates the ancestral and derived amino acids at the two sites distinguishing the pond and lake alleles suggests that D . pulicaria inherited the derived states from the D . tenebrosa ancestry. Our results suggest that some adaptations restricting the gene flow between D . pulicaria and D . pulex might have evolved in response to selection in ancestral environments rather than in the species’ current sympatric habitats. The Arctic ( D . tenebrosa ) populations are likely to provide important clues about these issues.