Morphological and molecular species boundaries in the Hyalella species flock of Lake Titicaca (Crustacea: Amphipoda)

Abstract

The Hyalella species diversity in the high-altitude water bodies of the Andean Altiplano is addressed using mitochondrial cox1 sequences and implementing different molecular species delimitation criteria. We have recorded the presence of five major genetic lineages in the Altiplano, of which one seems to be exclusive to Lake Titicaca and nearby areas, whereas the rest occur also in other regions of South America. Eleven out of 36 South American entities diagnosed by molecular delimitation criteria in our study are likely endemic to the Titicaca and neighbouring water bodies. We have detected a remarkable disagreement between morphology and genetic data in the Titicacan Hyalella, with occurrence of several cases of the same morpho-species corresponding to several Molecular Operational Taxonomic Units (MOTUs), some even distantly related, and other instances where a particular MOTU is shared by a morphologically heterogeneous array of species, including species with body smooth and others with body heavily armoured. Species diversification and incongruence between morphological and molecular boundaries within this species assemblage may be associated to the sharp changes in hydrological conditions experienced by the water bodies of the Altiplano in the past, which included dramatic fluctuations in water level and salinity of Lake Titicaca. Such environmental shifts could have triggered rapid morphological changes and ecological differentiation within the Hyalella assemblage, followed by phenotypic convergence among the diverse lineages. Factors such as phenotypic plasticity, incomplete lineage sorting or admixture between divergent lineages might lie also at the root of the morphological-genetic incongruence described herein.

Phylogenomics of the Hyalella amphipod species-flock of the Andean Altiplano

“…( c ) MSC tree based on single-copy nuclear gene-fragments plus the 13 mitochondrial protein-coding genes as an extra “gene”. For both ( b , c ) the terminals were classified into species following results by Jurado-Rivera et al 15 , letters and numbers on tips refer to Molecular Taxonomic Operational Units. Trees are available in nexus format in the GitHub repository ( https://github.com/Frazapel/Hyalella-amphipod-Phylogenomics ).…”

“…We also uncovered a disagreement between morphology and genetic data in the Titicacan Hyalella , with cases of same morpho-species displaying very distinct mitochondrial haplotypes, while others diagnosed as belonging to the same cox1 molecular operational taxonomic unit (MOTU). No significant discordances between mitochondrial and nuclear data were observed in Titicacan amphipods by either the Adamowicz et al 14 or Jurado-Rivera et al 15 surveys. Morphological conflict with molecular phylogenies has also been detected in amphipods of ancient Lake Baikal 21 .…”

“…Nuclear and mitochondrial phylogenomic analyses strongly support the hypothesis that the Titicaca species-flock originated from multiple colonization events from independent Hyalella ancestral lineages, with clades not showing marked relationships to particular sub-basins or regions in the main Lake or adjacent water bodies. Previous results using a short mitochondrial gene fragment ( cox1 ) on a broad South American sampling of the genus pointed to the occurrence of at least five major distant monophyletic clades in the Titicaca and other waterbodies in the northern Altiplano 14 , 15 . Clades A, B, C and E were shown to be part of lineages displaying a wider South American distribution, while members of clade D were exclusive of the Altiplano 15 .…”

“…Previous studies using mitochondrial cytochrome c oxidase subunit I ( cox1 ) DNA sequences supplemented with a nuclear marker demonstrated that the Hyalella in the Titicaca are polyphyletic, and divide into five major genetic lineages embedded in the broader South American Hyalella phylogeny 14 , 15 . Several independent colonizations deriving from South American lineages that diverged from each other in the last 15–20 My seem to have populated the Andean Altiplano, with evidence of the occurrence of intra-lacustrine diversification detected in at least two of the clades 14 , 15 . In a previous work, we applied molecular species delimitation criteria concluding that at least one-third of the Hyalella species diagnosed in that study are likely endemic to the Titicaca and neighbouring water bodies 15 .…”

“…Several independent colonizations deriving from South American lineages that diverged from each other in the last 15–20 My seem to have populated the Andean Altiplano, with evidence of the occurrence of intra-lacustrine diversification detected in at least two of the clades 14 , 15 . In a previous work, we applied molecular species delimitation criteria concluding that at least one-third of the Hyalella species diagnosed in that study are likely endemic to the Titicaca and neighbouring water bodies 15 . We also uncovered a disagreement between morphology and genetic data in the Titicacan Hyalella , with cases of same morpho-species displaying very distinct mitochondrial haplotypes, while others diagnosed as belonging to the same cox1 molecular operational taxonomic unit (MOTU).…”