Evolution of male pregnancy associated with remodeling of canonical vertebrate immunity in seahorses and pipefishes

Abstract

A fundamental problem for the evolution of pregnancy, the most specialized form of parental investment among vertebrates, is the rejection of the nonself-embryo. Mammals achieve immunological tolerance by down-regulating both major histocompatibility complex pathways (MHC I and II). Although pregnancy has evolved multiple times independently among vertebrates, knowledge of associated immune system adjustments is restricted to mammals. All of them (except monotremata) display full internal pregnancy, making evolutionary reconstructions within the class mammalia meaningless. Here, we study the seahorse and pipefish family (syngnathids) that have evolved male pregnancy across a gradient from external oviparity to internal gestation. We assess how immunological tolerance is achieved by reconstruction of the immune gene repertoire in a comprehensive sample of 12 seahorse and pipefish genomes along the “male pregnancy” gradient together with expression patterns of key immune and pregnancy genes in reproductive tissues. We found that the evolution of pregnancy coincided with a modification of the adaptive immune system. Divergent genomic rearrangements of the MHC II pathway among fully pregnant species were identified in both genera of the syngnathids: The pipefishes (Syngnathus) displayed loss of several genes of the MHC II pathway while seahorses (Hippocampus) featured a highly divergent invariant chain (CD74). Our findings suggest that a trade-off between immunological tolerance and embryo rejection accompanied the evolution of unique male pregnancy. That pipefishes survive in an ocean of microbes without one arm of the adaptive immune defense suggests a high degree of immunological flexibility among vertebrates, which may advance our understanding of immune-deficiency diseases.

The genomic timeline of cichlid fish diversification across continents

“…We assessed the robustness of our divergence-time estimates with a range of re-analyses that were identical to those with the “strict” dataset except that (1) MCMC sampling was done without data, only from the prior distributions; (2) all cichlid fossils were excluded; (3) the fossil sampling rate assumed for CladeAge calibrations was doubled or halved; (4) the net diversification rate assumed for calibrations was doubled or halved; or (5) the interrelationship of Osteoglossomorpha, Elopomorpha, and Clupeocephala (all remaining teleosts) was constrained so that Osteoglossomorpha were either the sister group to Elopomorpha 14 , 74 or to Clupeocephala 12 , 19 .…”

Genome sequences reveal global dispersal routes and suggest convergent genetic adaptations in seahorse evolution

“…1 , Figshare: Dataset 1 ). All seahorses are sedentary but exhibit specialized morphological and life-history traits 11 – 13 , such as a prehensile tail (and the lack of a caudal fin), an elongated snout, lack of pelvic fins, an armor of bony plates instead of scales, and a unique mode of male pregnancy whereby males give birth to developed juveniles 14 , 15 . Species of seahorses differ widely in body size, color patterns and other adaptive traits to their respective environments 11 , such as the presence or absence of bony spines, which are likely an adaption against predators 16 .…”

Supergene origin and maintenance in Atlantic cod

“…Targeted assembly was conducted with Kollector v.1.0.1 [99], using marker sequences of Gadus morhua from Roth et al [98] as queries. From the set of whole-genome and targeted assemblies, candidate orthologs to the 3,061 exon markers used by Roth et al [98] were then identified through TBLASTN searches, using sequences of Danio rerio as queries as in the earlier study. The identified sequences were aligned with MAFFT and filtered to exclude potentially remaining paralogous sequences and misaligned regions: We removed all sequences with TBLASTN bitscore values below 0.9× the highest bitscore value and all sequences that had dN/dS values greater than 0.3 in comparison to the Danio rerio queries, we removed codons from the alignment for which BMGE v.1.1 [100] determined a gap rate greater than 0.2 or an entropy-like score greater than 0.5, and we excluded exon alignments with a length shorter than 150 bp, more than two missing sequences, or a GC-content standard deviation greater than 0.04.…”