Transcriptome‐based phylogeny of endemic Lake Baikal amphipod species flock: fast speciation accompanied by frequent episodes of positive selection

Abstract

Endemic species flocks inhabiting ancient lakes, oceanic islands and other long-lived isolated habitats are often interpreted as adaptive radiations. Yet molecular evidence for directional selection during species flocks radiation is scarce. Using partial transcriptomes of 64 species of Lake Baikal (Siberia, Russia) endemic amphipods and two nonendemic outgroups, we report a revised phylogeny of this species flock and analyse evidence for positive selection within the endemic lineages. We confirm two independent invasions of amphipods into Baikal and demonstrate that several morphological features of Baikal amphipods, such as body armour and reduction in appendages and sensory organs, evolved in several lineages in parallel. Radiation of Baikal amphipods has been characterized by short phylogenetic branches and frequent episodes of positive selection which tended to be more frequent in the early phase of the second invasion of amphipods into Baikal when the most intensive diversification occurred. Notably, signatures of positive selection are frequent in genes encoding mitochondrial membrane proteins with electron transfer chain and ATP synthesis functionality. In particular, subunits of both the membrane and substrate-level ATP synthases show evidence of positive selection in the plankton species Macrohectopus branickii, possibly indicating adaptation to active plankton lifestyle and to survival under conditions of low temperature and high hydrostatic pressures known to affect membranes functioning. Other functional categories represented among genes likely to be under positive selection include Ca-binding muscle-related proteins, possibly indicating adaptation to Ca-deficient low mineralization Baikal waters.

Bursts of amino acid replacements in protein evolution

“…Genes that harbored bursts are enriched in mitochondrial proteins: they constitute 3 of the 5 such genes, although only 14% of the initial set of COGs are annotated as components of mitochondria (binomial test, p-value = 0.02); Supplementary Fig. 3) (Naumenko et al, 2017). No significant synonymous bursts were observed.…”

“…We searched for bursts of amino acid substitutions ("bursts") within internal edges of phylogenetic trees that are shorter than 0.005 dS. Suitable edges are present in 5 clades of the phylogenetic tree of gammarids from the Lake Baikal (Naumenko et al, 2017): Eulimnogammarus and related genera (18 edges), Pallasea and related genera (10), Hyallelopsis (3), Acanthogammaridae s. str. (7), and Micruropidae (4); as well as within the Catarrini clade (3 edges) of the tree of vertebrates ( Supplementary Fig.…”

“…Presumptive functions of amphipod genes were inferred from blast2GO predictions (Naumenko et al, 2017) and from the genome annotation of a related species Hyalella azteca (BCM-HGSC); functions of primate genes were inferred the human genome annotation (hg38).…”

“…Fortunately, it may be possible to identify such bursts indirectly, through comparison of genomes of extant species, as long as their phylogenetic tree contains very short internal edges. We took advantage of two phylogenetic trees that meet this requirement, those of the Lake Baikal amphipods (Naumenko et al, 2017) and of Catarrhini (Rosenbloom et al, 2015, UCSC 100 vertebrates multiple alignment), and investigated short bursts in the evolution of their proteins.…”

Symbiosis, Selection and Novelty: Freshwater Adaptation in the Unique Sponges of Lake Baikal

“…This has lead to the investigation of a number of Baikal species using next-generation sequencing (e.g. Rivarola-Duarte et al 2014, Romanova et al 2016, Naumenko et al 2017.…”