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Fish lateral line innovation: insights into the evolutionary genomic dynamics of a unique mechanosensory organ - PubMed

Comparative Study

. 2012 Dec;29(12):3887-98.

doi: 10.1093/molbev/mss194. Epub 2012 Jul 27.

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Comparative Study

Fish lateral line innovation: insights into the evolutionary genomic dynamics of a unique mechanosensory organ

Siby Philip et al. Mol Biol Evol. 2012 Dec.

Abstract

The mechanosensory lateral line, found only in fishes and amphibians, is an important sense organ associated with aquatic life. Lateral line patterns differ among teleost, the most diverse vertebrate taxa, hypothetically in response to selective pressures from different aquatic habitats. In this article, we conduct evolutionary genomic analyses of 34 genes associated with lateral line system development in teleosts to elucidate the significance of contrasting evolutionary rates and changes in the protein coding sequences. We find that duplicated copies of these genes are preferentially retained in the teleost genomes and that episodic events of positive selection have occurred in 22 of the 30 postduplication branches. In general, teleost genes evolved at a faster rate relative to their tetrapod counterparts, and the mutation rates of 26 of the 34 genes differed among teleosts and tetrapods. We conclude that following whole genome duplication, evolutionary rates and episodic events of positive selection on the lateral line system development genes might have been one of the factors favoring the subsequent adaptive radiation of teleosts into diverse habitats. These results provide the foundation for further detailed explorations into lateral line system genes and the evolution of diverse phenotypes and adaptations.

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Figures

F<sc>ig</sc>. 1.
Fig. 1.

Schematic representation of the ALL and PLL. (A) ALL and PLLs are highlighted on Albumus albumus. (B) Schematic representation of the lateral line canal system. (C) Structure of a single neuromast. (D) Representative teleosts with different lateral line patterns are shown: (i) Microinchthys sanzoni, (ii) Carangoides hedlandensis, (iii) Cynoglossus cynoglossus, (iv) Cyttopsis rosea, (v) Cheilopogon spilopterus, and (vi) Grammatonotus crosnieri. (Note that there are many other patterns of lateral lines and there are some species with PLL completely absent or truncated.)

F<sc>ig</sc>. 2.
Fig. 2.

The results of rate-shift analysis on the postduplication branches. (A) Schematic representation of a phylogenetic tree showing rate shift in only one postduplication branch. (B) Schematic representation of the phylogenetic tree where both the postduplication branches faced rated shift. (C) Rose window representation of the strict FSGD duplicates in zebrafish plotted. Sets of genes in each models of rate-shift are shaded similar to the model tree; cxcl12a has no rate-shift in its postduplication branches.

F<sc>ig.</sc> 3.
Fig. 3.

Cumulative distribution frequency of the CONACC scores for the (A) teleost subtree and (B) whole tree; the plots shows a significant skew of the CONACC scores for teleosts toward less than zero (<0), which indicates acceleration of evolution.

F<sc>ig</sc>. 4.
Fig. 4.

The results of the compartmentalization analysis. All five phases (A–E) are shown, and the genes selected in each phase are listed beside the tree. The three compartments used for the analysis are labeled on the tree, and differences in evolutionary rates are shaded differently. Note that SelectionLRT.bf considers the separating branch as a single compartment, so the two branches emanating from the root form a single branch in this analysis.

F<sc>ig</sc>. 5.
Fig. 5.

Schematic representation of episodic positive selection in CXCR4, which was duplicated in teleosts during FSGD. Only the branch leading to cxcr4b in teleosts had signal of positive selection based on the branch-site model in PAML, and teleost terminal branches showed no positive selection in the branch-site model comparison. (Positively selected sites on the ancestral branch leading to the teleost cxcr4b paralog are 30V, 44G, 109T, 145L, 151G, 295Y, 321S, 325R, 326S, 327S, 328H, 329K, and 332T.)

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