Genomics and the origin of marine species

The work within this doctoral thesis introduces the Caribbean reef fish genus Hypoplectrus (hamlets) into the field of speciation genomics. The overarching theme within this thesis is the investigation of the underlying evolutionary drivers that are acting at the origin of this marine radiation and facilitate rapid speciation within the ocean. Distributed over four separate manuscripts, this work addresses several aspects impacting the dynamics of the Hypoplectrus radiation. Within the first manuscript, the temporal stability of the hamlet community in a patch of reefs in Puerto Rico is investigated. The findings indicate that the hamlet community composition is dynamic and potentially impacted by ecological factors such as turbidity or the presence of specific coral species. Within the second manuscript the hamlet reference genome is introduced and whole genome resequencing is applied to investigate the signals of speciation within three of the most common hamlet species. The results show that, against a genome wide background of very low differentiation, a small number of color pattern and vision genes are highly differentiated between species and apparently co-selected for. The third manuscript explores the demographic history of a rare endemic hamlet species. It uses a coalescent approach to show the decline in population size of this particular species since the recent evolutionary split from the remaining genus. In the last manuscript, nine different hamlet species are sequenced to provide a cross section through the hamlet radiation. The results of population- and phylogenomics indicate ongoing inter-species gene flow throughout the majority of the genome with only a small set of putative barrier genes. Phylogenetic relationships through most of the genome are diffuse, yet the signal within the few differentiated genomic intervals is discordant, pointing to introgession events or differential lineage sorting at those major effect loci

Rapid radiation in a highly diverse marine environment

Significance: Adaptive radiation, the evolutionary process whereby a lineage diversifies over a short period of time, often occurs in geographically isolated or newly formed habitats where colonizing species encounter unoccupied niches and reduced selective pressures. Rapid radiations may also occur in diverse and complex environments, but these cases are less well documented. Here, we show that the hamlets, a group of Caribbean reef fishes, radiated within the last 10,000 generations in a burst of diversification that ranks among the fastest in fishes. Genomic analysis suggests that color pattern diversity is generated by different combinations of alleles at a few genes with large effect. Such a modular genomic architecture of diversification is emerging as a common denominator to a variety of radiations. Abstract: Rapid diversification is often observed when founding species invade isolated or newly formed habitats that provide ecological opportunity for adaptive radiation. However, most of the Earth’s diversity arose in diverse environments where ecological opportunities appear to be more constrained. Here, we present a striking example of a rapid radiation in a highly diverse marine habitat. The hamlets, a group of reef fishes from the wider Caribbean, have radiated into a stunning diversity of color patterns but show low divergence across other ecological axes. Although the hamlet lineage is ∼26 My old, the radiation appears to have occurred within the last 10,000 generations in a burst of diversification that ranks among the fastest in fishes. As such, the hamlets provide a compelling backdrop to uncover the genomic elements associated with phenotypic diversification and an excellent opportunity to build a broader comparative framework for understanding the drivers of adaptive radiation. The analysis of 170 genomes suggests that color pattern diversity is generated by different combinations of alleles at a few large-effect loci. Such a modular genomic architecture of diversification has been documented before in Heliconius butterflies, capuchino finches, and munia finches, three other tropical radiations that took place in highly diverse and complex environments. The hamlet radiation also occurred in a context of high effective population size, which is typical of marine populations. This allows for the accumulation of new variants through mutation and the retention of ancestral genetic variation, both of which appear to be important in this radiation

Rapid radiation in a highly diverse marine environment

Hench K, Helmkampf M, McMillan WO, Puebla O. Rapid radiation in a highly diverse marine environment. Proceedings of the National Academy of Sciences. 2022;119(4).**Significance** Adaptive radiation, the evolutionary process whereby a lineage diversifies over a short period of time, often occurs in geographically isolated or newly formed habitats where colonizing species encounter unoccupied niches and reduced selective pressures. Rapid radiations may also occur in diverse and complex environments, but these cases are less well documented. Here, we show that the hamlets, a group of Caribbean reef fishes, radiated within the last 10,000 generations in a burst of diversification that ranks among the fastest in fishes. Genomic analysis suggests that color pattern diversity is generated by different combinations of alleles at a few genes with large effect. Such a modular genomic architecture of diversification is emerging as a common denominator to a variety of radiations.Rapid diversification is often observed when founding species invade isolated or newly formed habitats that provide ecological opportunity for adaptive radiation. However, most of the Earth’s diversity arose in diverse environments where ecological opportunities appear to be more constrained. Here, we present a striking example of a rapid radiation in a highly diverse marine habitat. The hamlets, a group of reef fishes from the wider Caribbean, have radiated into a stunning diversity of color patterns but show low divergence across other ecological axes. Although the hamlet lineage is ∼26 My old, the radiation appears to have occurred within the last 10,000 generations in a burst of diversification that ranks among the fastest in fishes. As such, the hamlets provide a compelling backdrop to uncover the genomic elements associated with phenotypic diversification and an excellent opportunity to build a broader comparative framework for understanding the drivers of adaptive radiation. The analysis of 170 genomes suggests that color pattern diversity is generated by different combinations of alleles at a few large-effect loci. Such a modular genomic architecture of diversification has been documented before inHeliconiusbutterflies, capuchino finches, and munia finches, three other tropical radiations that took place in highly diverse and complex environments. The hamlet radiation also occurred in a context of high effective population size, which is typical of marine populations. This allows for the accumulation of new variants through mutation and the retention of ancestral genetic variation, both of which appear to be important in this radiation

Raw transect data on hamlet abundances at reefs of La Parguera (Puerto Rico) in March 2017

The data sheet contains the individual counts of seven hamlet species (Hypoplectrus spp.) observed within transects at Puerto Rican coral reefs. The data is based on a series of SCUBA based transects conducted during March 2017. Each row contains the hamlet counts of a single 400 m² transect

Temporal changes in hamlet communities (Hypoplectrus spp., Serranidae) over 17 years

Transect surveys of hamlet communities (Hypoplectrus spp., Serranidae) covering 14 000 m2 across 16 reefs off La Parguera, Puerto Rico, are presented and compared with a previous survey conducted in the year 2000. The hamlet community has noticeably changed over 17 years, with a > 30% increase in relative abundance of the yellowtail hamlet Hypoplectrus chlorurus on the inner reefs at the expense of the other hamlet species. The data also suggest that the density of H. chlorurus has declined and that its distribution has shifted towards shallower depths. Considering that H. chlorurus has been previously identified as one of the few fish showing a positive association with seawater turbidity on the inner reefs of La Parguera and that sedimentation of terrestrial origin has increased over recent decades on these reefs, it is proposed that turbidity may constitute an important but so far overlooked ecological driver of hamlet communities

Phased genotypes of Caribbean reef fishes (Hypoplectrus sp.)

Genotypes of 110 hamlets (H. nigricans, H. puella and H. unicolor). Based on ~24x Illumina sequencing data, created with GATK and phased using SHAPEIT