Bimodal evolution of the killer cell Ig-like receptor (KIR) family in New World primates

Cadavid, Luis F.; Palacios, Catalina; Lugo, Juan S.

doi:10.1007/s00251-013-0719-4

Cited by 8 publications

(12 citation statements)

References 38 publications

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“…Our results echo findings from different immunogenetic contexts; for example, episodic positive selection was found to play a key role in the evolution of killer cell Ig-like receptor sequences in New World primates [22] and in the evolution of a cluster of disease-response genes within the Poaceae (true grasses) [52]. Avian TLR4 had the second-highest proportion of positively-selected codons (after TLR5 , Table 1), concordant with an observation that TLR4 showed a higher degree of episodic selection than TLR7 in rats and mice [8].…”

Section: Discussionsupporting

confidence: 88%

Episodic Positive Selection in the Evolution of Avian Toll-Like Receptor Innate Immunity Genes

2014

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Toll-like receptors (TLRs) are a family of conserved pattern-recognition molecules responsible for initiating innate and acquired immune responses. Because they play a key role in host defence, these genes have received increasing interest in the evolutionary and population genetics literature, as their variation represents a potential target of adaptive evolution. However, the role of pathogen-mediated selection (i.e. episodic positive selection) in the evolution of these genes remains poorly known and has not been examined outside of mammals. A recent increase in the number of bird species for which TLR sequences are available has enabled us to examine the selective processes that have influenced evolution of the 10 known avian TLR genes. Specifically, we tested for episodic positive selection to identify codons that experience purifying selection for the majority of their evolution, interspersed with bursts of positive selection that may occur only in restricted lineages. We included up to 23 species per gene (mean = 16.0) and observed that, although purifying selection was evident, an average of 4.5% of codons experienced episodic positive selection across all loci. For four genes in which sequence coverage traversed both the extracellular leucine-rich repeat region (LRR) and transmembrane/intracellular domains of the proteins, increased positive selection was observed at the extracellular domain, consistent with theoretical predictions. Our results provide evidence that episodic positive selection has played an important role in the evolution of most avian TLRs, consistent with the role of these loci in pathogen recognition and a mechanism of host-pathogen coevolution.

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Section: Discussionsupporting

confidence: 88%

Episodic Positive Selection in the Evolution of Avian Toll-Like Receptor Innate Immunity Genes

2014

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“…Episodic selection has been frequently linked with coevolutionary dynamics, and is generally consistent with the evolutionary forces that may be imposed by shifts between different selective environments, including host shifts in immunogenic contexts ( Rech et al. 2012 ; Cadavid et al. 2013 ; Murray et al.…”

Section: Discussionmentioning

confidence: 82%

Piercing Fishes: Porin Expansion and Adaptation to Hematophagy in the Vampire Snail Cumia reticulata

Gerdol

Cervelli

Oliverio

et al. 2018

Molecular Biology and Evolution

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Cytolytic pore-forming proteins are widespread in living organisms, being mostly involved in both sides of the host–pathogen interaction, either contributing to the innate defense or promoting infection. In venomous organisms, such as spiders, insects, scorpions, and sea anemones, pore-forming proteins are often secreted as key components of the venom. Coluporins are pore-forming proteins recently discovered in the Mediterranean hematophagous snail Cumia reticulata (Colubrariidae), highly expressed in the salivary glands that discharge their secretion at close contact with the host. To understand their putative functional role, we investigated coluporins’ molecular diversity and evolutionary patterns. Coluporins is a well-diversified family including at least 30 proteins, with an overall low sequence similarity but sharing a remarkably conserved actinoporin-like predicted structure. Tracking the evolutionary history of the molluscan porin genes revealed a scattered distribution of this family, which is present in some other lineages of predatory gastropods, including venomous conoidean snails. Comparative transcriptomic analyses highlighted the expansion of porin genes as a lineage-specific feature of colubrariids. Coluporins seem to have evolved from a single ancestral porin gene present in the latest common ancestor of all Caenogastropoda, undergoing massive expansion and diversification in this colubrariid lineage through repeated gene duplication events paired with widespread episodic positive selection. As for other parasites, these findings are congruent with a “one-sided arms race,” equipping the parasite with multiple variants in order to broaden its host spectrum. Overall, our results pinpoint a crucial adaptive role for coluporins in the evolution of the peculiar trophic ecology of vampire snails.

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“…None of the catarrhine KIR lineages is represented in the platyrrhine primates, who have their own unique lineage VI KIR . The sequence and organization of KIR haplotypes from owl monkey and spider monkey, species representing two of the five families of New World monkeys, have been examined . The spider monkey haplotype has five functional KIR genes with a pseudogene at the centromeric end of the locus and FCAR flanking the telomeric end.…”

Section: Kir Genes Of Catarrhine and Platyrrhine Primates Are More DImentioning

confidence: 99%

“…These KIR4DL have two D0 domains. Extensive KIR gene diversity and polymorphism characterize both the owl monkey and spider monkey KIR locus .…”

Section: Kir Genes Of Catarrhine and Platyrrhine Primates Are More DImentioning

confidence: 99%

Co‐evolution of MHC class I and variable NK cell receptors in placental mammals

Guethlein

Norman

Hilton

et al. 2015

Immunological Reviews

140

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Summary Shaping natural killer (NK) cell functions in human immunity and reproduction are diverse killer-cell immunoglobulin-like receptors (KIRs) that recognize polymorphic MHC class I determinants. A survey of placental mammals suggests KIRs serve as variable NK cell receptors only in certain primates and artiodactyls. Divergence of functional and variable KIRs in primates and artiodactyls predates placental reproduction. Among artiodactyls, cattle but not pigs have diverse KIRs. Catarrhine (humans, apes, and Old World monkeys) and platyrrhine (New World monkeys) primates, but not prosimians, have diverse KIRs. Platyrrhine and catarrhine systems of KIR and MHC class I are highly diverged, but within the catarrhines a stepwise co-evolution of MHC class I and KIRs is discerned. In Old World monkeys, diversification focuses on MHC-A and MHC-B and their cognate lineage II KIR. With evolution of C1-bearing MHC-C from MHC-B, as informed by orangutan, the focus changes to MHC-C and its cognate lineage III KIR. Evolution of C2 from C1 and fixation of MHC-C, drove further elaboration of MHC-C-specific KIRs, as exemplified by chimpanzee. In humans, the evolutionary trajectory changes again. Emerging from reorganization of the KIR locus and selective attenuation of KIR avidity for MHC class I are the functionally distinctive KIR A and KIR B haplotypes.

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Bimodal evolution of the killer cell Ig-like receptor (KIR) family in New World primates

Cited by 8 publications

References 38 publications

Episodic Positive Selection in the Evolution of Avian Toll-Like Receptor Innate Immunity Genes

Episodic Positive Selection in the Evolution of Avian Toll-Like Receptor Innate Immunity Genes

Piercing Fishes: Porin Expansion and Adaptation to Hematophagy in the Vampire Snail Cumia reticulata

Co‐evolution of MHC class I and variable NK cell receptors in placental mammals

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