Genome assemblies and genetic maps highlight chromosome-scale macrosynteny in Atlantic acroporids

Abstract

Background: Corals belong to the Cnidaria, an early branching phylum of metazoans. Over the course of their long evolutionary history, they have adapted to changing environments, such as rising sea levels and increasing ocean temperatures. While their history speaks to their evolutionary capacity, it is less clear how quickly they may respond to rapid changes. A critical aspect of adaptive capacity is the structure of their genome and the genetic diversity contained within. Findings: Here, we present chromosome-scale genome assemblies and genetic linkage maps of two critically endangered coral species, Acropora palmata and A. cervicornis, the two extant Atlantic acroporid corals. Genomes of both species were resolved into 14 chromosomes with comparable assembly sizes (A. palmata, 287Mb; A. cervicornis, 305Mb). Gene content, repeat content, gene collinearity and macrosynteny were largely preserved between the Atlantic acroporids but a 2.5 Mb inversion and 1.4 Mb translocation were detected between two of the chromosome pairs. Macrosynteny and gene collinearity decreased when comparing Atlantic with Pacific acroporids. Paracentric inversions of whole chromosome arms characterized A. hyacinthus, specifically. In the larger context of cnidarian evolution, the four acroporids and another scleractinian coral with chromosome-resolved genome assemblies retained six of 21 cnidarian ancestral linkage groups, while also privately sharing numerous ALG fission and fusion events compared to other distantly related cnidarians. Genetic linkage maps were built using a 30K genotyping array with 105 offspring in one family for A. palmata and 154 offspring across 16 families for A. cervicornis. The A. palmata consensus linkage map spans 1,013.42 cM and includes 2,114 informative markers. The A. cervicornis consensus map spans 927.36 cM across 4,859 markers. A. palmata and A. cervicornis exhibited similarly high sex-averaged genome-wide recombination rates (3.53 cM/Mb and 3.04 cM/Mb, respectively) relative to other animals. In our gamete-specific maps, we found pronounced sex-based differences in recombination, known as heterochiasmy, in this simultaneous hermaphrodite, with both species showing recombination rates 2-2.5X higher in eggs compared to sperm. Conclusions: The genomic resources presented here are the first of their kind available for Atlantic coral species. These data sets revealed that adaptive capacity of endangered Atlantic corals is not limited by their recombination rates, with both species exhibiting high recombination rates and heterochiasmy. Nevertheless, the two sister species maintain high levels of macrosynteny and gene collinearity between them. The few large-scale rearrangements detected deserve further study as a potential cause of fertilization barriers between the species. Together, the assemblies and genetic maps presented here now enable genome-wide association studies and discovery of quantitative trait loci; tools that can aid in the conservation of these endangered corals.

Competing Interest Statement

The authors have declared no competing interest.