High-Quality Genome Assembly and Demographic History of the King Angelfish (Holacanthus passer), an Iconic Marine Fish of the Tropical Eastern Pacific

Core Concepts

The study presents the first high-quality annotated genome assembly of the King Angelfish (Holacanthus passer), a key marine fish species in the Tropical Eastern Pacific. The genome assembly and demographic history analysis provide insights into the evolutionary dynamics and population expansions of this iconic species.

Abstract

The study presents the first annotated genome assembly of the King Angelfish (Holacanthus passer), a prominent marine fish species in the Tropical Eastern Pacific (TEP). The researchers generated 43.8 Gb of Oxford Nanopore and 97.3 Gb of Illumina sequencing data, which provided 75X and 167X coverage, respectively, of the 583 Mb genome. The final assembly had a contig N50 of 5.7 Mb and captured 97.5% of the Actinopterygii Benchmarking Universal Single-Copy Orthologs (BUSCOs).
The genome annotation identified 33,889 protein-coding genes, of which 22,984 were functionally annotated. Repeat content analysis showed that repetitive elements account for 5.09% of the genome.
The demographic history analysis using the Pairwise Sequentially Markovian Coalescent (PSMC) model revealed two potential scenarios for the population dynamics of H. passer in the TEP. Considering a faster mutation rate (10^-8), the population showed a slow expansion around 300 Kya, followed by a rapid expansion 30 Kya. With a slower mutation rate (10^-9), the population exhibited an initial expansion around 2.8 Mya, a small decline around 600 Kya, and a subsequent rapid expansion 300 Kya.
These results suggest that the demographic history of H. passer was likely shaped by historical events associated with the closure of the Isthmus of Panama, rather than the more recent Last Glacial Maximum. This contrasts with most marine species, which typically show population expansions after the Last Glacial Maximum. The high-quality genome assembly and insights into the demographic history of this iconic TEP species will facilitate further research into local adaptation, speciation, and introgression in marine fishes.

Stats

The genome size of H. passer was estimated to be 579 Mb using GenomeScope analysis of Illumina k-mers.
The final assembled genome size was 583 Mb, with a contig N50 of 5.7 Mb.
Repetitive elements account for 5.09% of the H. passer genome.
The PSMC analysis suggested population expansions of H. passer prior to the Last Glacial Maximum, in contrast to most marine species.
The maximum effective population size was estimated to be around 300,000 individuals (using a mutation rate of 10^-8) or 2,800,000 individuals (using a mutation rate of 10^-9).

Quotes

"Our results support previous findings of marine population expansions in the TEP occurring prior to the LGM [Last Glacial Maximum]."
"This pattern is consistent with our analyses using both slow and fast mutation rates for H. passer, which showed population expansions beyond 30 Kya."
"Overall, drops in sea level decrease the available marine habitat, potentially restricting gene flow between populations, thus resulting in population bottlenecks."

Key Insights Distilled From

Whole genome assembly and annotation of the King Angelfish (Holacanthus passer) gives insight into the evolution of marine fishes of the Tropical Eastern Pacific

by Gatins,R., A... at www.biorxiv.org 11-10-2023

https://www.biorxiv.org/content/10.1101/2023.11.08.566026v1

Deeper Inquiries

How do the demographic histories of other marine species in the Tropical Eastern Pacific compare to the patterns observed in H. passer?

The demographic histories of other marine species in the Tropical Eastern Pacific (TEP) show similar patterns of population expansions preceding the Last Glacial Maximum (LGM), as observed in H. passer. Studies on various marine organisms in the TEP have reported population expansions that occurred prior to the LGM, indicating a common trend in the region. For example, species like the goby Elacatinus puncticulatus and the clingfish Gobieosox adustus experienced population expansions around 170-130 Kya and 200-150 Kya, respectively. Additionally, the reef fish Anisotremus interruptus showed population expansions in its continental populations after the LGM, around 5 Kya, while populations from oceanic islands like Revillagigedos and the Galapagos Archipelago experienced earlier expansions at around 55 Kya. These findings suggest a consistent pattern of demographic history in marine organisms of the TEP, with many species exhibiting population expansions predating the LGM.

What are the potential evolutionary mechanisms that could have led to the population expansions of H. passer prior to the Last Glacial Maximum, in contrast to the typical post-LGM expansions observed in many other marine organisms?

The population expansions of H. passer prior to the Last Glacial Maximum (LGM) could be attributed to several potential evolutionary mechanisms specific to the species and the environmental conditions in the Tropical Eastern Pacific (TEP). One possible mechanism is the historical events associated with the closure of the Isthmus of Panama, which could have influenced the genetic divergence and demographic history of H. passer. The separation of populations due to the closure of the Isthmus of Panama may have led to genetic isolation and subsequent population expansions as the species adapted to new environments and ecological niches.
Additionally, the availability of suitable habitats and ecological resources in the TEP could have facilitated population expansions in H. passer. The species' ability to adapt to diverse habitats, such as sponge feeding, herbivory, and fish cleaning interactions, may have contributed to its population growth and expansion over time. Furthermore, the unique social organization and reproductive strategies of H. passer, such as protogynous sequential hermaphroditism, could have played a role in promoting population growth and expansion.
Overall, the combination of historical events, ecological factors, and species-specific traits likely contributed to the population expansions of H. passer prior to the LGM, setting it apart from the typical post-LGM expansions observed in many other marine organisms.

What insights can the high-quality H. passer genome provide into the genomic basis of local adaptation, speciation, and introgression processes in marine fishes of the Tropical Eastern Pacific?

The high-quality genome of H. passer can provide valuable insights into the genomic basis of various evolutionary processes in marine fishes of the Tropical Eastern Pacific (TEP).

Local Adaptation: By analyzing the genomic data of H. passer, researchers can identify genetic variations associated with local adaptation to specific environmental conditions in the TEP. Understanding the genetic basis of traits related to habitat preferences, feeding behaviors, and reproductive strategies can shed light on the species' ability to thrive in diverse ecological niches.

Speciation: Comparative genomics studies using the H. passer genome can help elucidate the genetic mechanisms underlying speciation events in the TEP. By comparing genomic data across closely related species within the Holacanthus genus and other fish families, researchers can identify genomic regions associated with speciation and divergence processes.

Introgression: The genome of H. passer can also be used to study introgression events and hybridization dynamics in marine fishes of the TEP. By analyzing genetic admixture patterns and introgressed regions in the genome, researchers can investigate the extent of gene flow between different species and populations, providing insights into evolutionary relationships and hybridization outcomes.

Overall, the high-quality genome of H. passer serves as a valuable resource for studying the genomic basis of local adaptation, speciation, and introgression processes in marine fishes of the TEP, contributing to our understanding of evolutionary dynamics in this ecologically diverse region.