Abstract
Host-intrinsic factors as well as environmental changes are known to be strong evolutionary drivers defining the genetic foundation of immunity. Using a novel set of teleost genomes and a time-calibrated phylogeny, we here investigate the family of Toll-like receptor (TLR) genes and address the underlying evolutionary processes shaping the diversity of the first-line defence. Our findings reveal remarkable flexibility within the evolutionary design of teleost innate immunity characterized by prominent TLR gene losses and expansions. In the order of Gadiformes, expansions correlate with the loss of major histocompatibility complex class II (MHCII) and diversifying selection analyses support that this has fostered new immunological innovations in TLRs within this lineage. In teleosts overall, TLRs expansions correlate with species latitudinal distributions and maximum depth. By contrast, lineage-specific gene losses overlap with well-described changes in palaeoclimate (global ocean anoxia) and past Atlantic Ocean geography. In conclusion, we suggest that the evolvability of the teleost immune system has most likely played a prominent role in the survival and successful radiation of this lineage.
Highlights
The evolutionary success of ray-finned fishes is characterized by large species radiations [1]
The discoveries of the genetic loss of the major histocompatibility complex (MHC) class II pathway in Atlantic cod (Gadus morhua) as well as the functional loss in the more distant broadnosed pipefish (Syngnathus typhle) [5,6] show that major histocompatibility complex class II (MHCII) is not crucial for the defence against pathogens and survival in some fish species. These findings are further supported in a recent study by Malmstrom et al [7], which demonstrated that the loss of MHCII is shared by the entire Gadiformes lineage
We discovered a new Toll-like receptor (TLR), here annotated as TLR21beta based on sequence homology, which is absent in all Paracanthopterygiian species with the exception of P. japonica, and Lampridiformes
Summary
The evolutionary success of ray-finned fishes (class Actinopterygii) is characterized by large species radiations [1]. The discoveries of the genetic loss of the major histocompatibility complex (MHC) class II pathway in Atlantic cod (Gadus morhua) as well as the functional loss in the more distant broadnosed pipefish (Syngnathus typhle) [5,6] show that MHCII is not crucial for the defence against pathogens and survival in some fish species. These findings are further supported in a recent study by Malmstrom et al [7], which demonstrated that the loss of MHCII is shared by the entire Gadiformes lineage.
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