Mitochondrial Capture Misleads about Ecological Speciation in the Daphnia pulex Complex

Abstract

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.

Reproduction of Daphnia pulex in a Northern Italy pond

“…Our results suggest that further investigation are advisable in order to verify whether the current population is the last remnant of a once much larger metapopulation eventually reduced by anthropogenic disturbances (e.g., fish introductions, water contamination with toxic chemicals) or if it represents the invasion of North American strains that have recently colonised large parts of New Zealand, Africa and Spain, and that was already recorded in Northern Italy and Sardinia (Mergeay et al, 2006; Vergilino et al, 2011;Duggan et al, 2012;Crease et al, 2012;Markova et al, 2013).…”

“…The identity of European and American populations of morphologically similar species may be doubtful (Hrbacek, 1987). The accumulation of genetic data has showed that North American and European D. pulex are genetically two distinct species and nomenclature of the D. pulex complex is not resolved (Colbourne et al, 1998;Palsoon, 2000;Mergeay et al, 2006;Petrusek et al, 2008;Crease et al, 2012;Markova et al, 2013). Even in Europe, asexual strains of D. pulex show a more northerly distribution than sexual ones (Ward et al, 1994;Weider and Hobaek, 1997) and both lineages may co-exist within the same geographical region (Letho and Haag, 2010).…”

“…D. pulex was recorded both in permanent and temporary habitats in Northern and Southern Italy (de Bernardi et al, 1985;Stoch et al, 2002;Marrone et al, 2007;Leoni and Garibaldi, 2009) and in several Italian islands: Sicily, Sardinia, Lampedusa and Capraia (Stoch et al, 2002;Marrone et al, 2006). By molecular markers, panarctic and North American D. pulex individuals were identified in Northern Italy and in Sardinia (Vergilino et al, 2011;Markova et al, 2013).…”

Seventy five years of limnology at the Istituto Italiano di Idrobiologia in Pallanza

“…To characterize the interactions of organisms with their environment at molecular level, genomics studies genetic material recovered directly from environmental samples, proteomic addresses protein localization and functional cataloguing, and metabolomics assesses organism function and health through metabolites dynamics. Methods frequently include using microsatellites to determine gene flow and hybridization between populations (Colautti et al, 2005;Vergilino et al, 2011;Marková et al, 2013). The development of molecular ecology is also closely related to the use of DNA microarrays, which allows for the simultaneous analysis of the expression of thousands of different genes.…”

Phenology of Daphnia in a Northern Italy pond during the weather anomalous 2014

“…The presence of the predaceous larvae of Chaoborus flavicans probably account for seasonal variation of juveniles morphology that showed neckteeth and/or elongated tail spines as typical predator- (Rossi et al, 2014). Recently, the invasive hybrid lineage of the American D. pulex and American D. pulicaria, invaded Africa and was already recorded in Northern Italy and Sardinia (Mergeay et al, 2006;Fadda et al, 2011;Marková et al, 2013). In this study, we used a diagnostic mitochondrial DNA gene to identify if D. pulex population from Bodrio del pastore III represents this invasive hybrid clone or if it belongs to native European D. pulex strain.…”