The Genomes of the Livebearing Fish Species Poeciliopsis retropinna and Poeciliopsis turrubarensis Reflect Their Different Reproductive Strategies

Abstract

The evolution of a placenta is predicted to be accompanied by rapid evolution of genes involved in processes that regulate mother–offspring interactions during pregnancy, such as placenta formation, embryonic development, and nutrient transfer to offspring. However, these predictions have only been tested in mammalian species, where only a single instance of placenta evolution has occurred. In this light, the genus Poeciliopsis is a particularly interesting model for placenta evolution, because in this genus a placenta has evolved independently from the mammalian placenta. Here, we present and compare genome assemblies of two species of the livebearing fish genus Poeciliopsis (family Poeciliidae) that differ in their reproductive strategy: Poeciliopsis retropinna which has a well-developed complex placenta and P. turrubarensis which lacks a placenta. We applied different assembly strategies for each species: PacBio sequencing for P. retropinna (622-Mb assembly, scaffold N50 of 21.6 Mb) and 10× Genomics Chromium technology for P. turrubarensis (597-Mb assembly, scaffold N50 of 4.2 Mb). Using the high contiguity of these genome assemblies and near-completeness of gene annotations to our advantage, we searched for gene duplications and performed a genome-wide scan for genes evolving under positive selection. We find rapid evolution in major parts of several molecular pathways involved in parent–offspring interaction in P. retropinna, both in the form of gene duplications as well as positive selection. We conclude that the evolution of the placenta in the genus Poeciliopsis is accompanied by rapid evolution of genes involved in similar genomic pathways as found in mammals.

Inflammation and convergent placenta gene co-option contributed to a novel reproductive tissue

“…Accordingly, genes have been recruited non-randomly for certain functions in convergent innovations, 40 , 41 , 42 , 43 , 44 , 45 , 46 including pregnancy and placentation in fishes, reptiles, and mammals. 47 , 48 , 49 , 50 , 51 , 52 , 53 Similar to mammalian placentation, plug development depends on well-coordinated cell proliferation, ECM formation, and angiogenesis. To explore whether genes with important roles in mammalian placentas were also recruited into the plug, we analyzed expression of 41 one-to-one orthologs of the mammalian core placenta transcriptome.…”

Molecular Signatures of Placentation and Secretion Uncovered in Poeciliopsis Maternal Follicles

“…A transcriptome mapping reference was made in Kallisto using the Kallisto index function ( Bray et al. 2016 ) on the coding sequence FASTA files from the P. retropinna (PRJNA555005) and P. turrubarensis (PRJNA555006) genomes ( van Kruistum et al. 2020 ).…”

Parallel Genomic Changes Drive Repeated Evolution of Placentas in Live-Bearing Fish

“…2018 ; van Kruistum et al. 2019 , 2020 ). However, these studies did not compare multiple instances of placenta evolution on a genome-wide scale, include closely related nonplacental species, or consider noncoding regions of the genome.…”