skip to main content


Title: Divergent sensory and immune gene evolution in sea turtles with contrasting demographic and life histories
Sea turtles represent an ancient lineage of marine vertebrates that evolved from terrestrial ancestors over 100 Mya. The genomic basis of the unique physiological and ecological traits enabling these species to thrive in diverse marine habitats remains largely unknown. Additionally, many populations have drastically declined due to anthropogenic activities over the past two centuries, and their recovery is a high global conservation priority. We generated and analyzed high-quality reference genomes for the leatherback ( Dermochelys coriacea ) and green ( Chelonia mydas ) turtles, representing the two extant sea turtle families. These genomes are highly syntenic and homologous, but localized regions of noncollinearity were associated with higher copy numbers of immune, zinc-finger, and olfactory receptor (OR) genes in green turtles, with ORs related to waterborne odorants greatly expanded in green turtles. Our findings suggest that divergent evolution of these key gene families may underlie immunological and sensory adaptations assisting navigation, occupancy of neritic versus pelagic environments, and diet specialization. Reduced collinearity was especially prevalent in microchromosomes, with greater gene content, heterozygosity, and genetic distances between species, supporting their critical role in vertebrate evolutionary adaptation. Finally, diversity and demographic histories starkly contrasted between species, indicating that leatherback turtles have had a low yet stable effective population size, exhibit extremely low diversity compared with other reptiles, and harbor a higher genetic load compared with green turtles, reinforcing concern over their persistence under future climate scenarios. These genomes provide invaluable resources for advancing our understanding of evolution and conservation best practices in an imperiled vertebrate lineage.  more » « less
Award ID(s):
1904439
NSF-PAR ID:
10436712
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; more » ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; « less
Date Published:
Journal Name:
Proceedings of the National Academy of Sciences
Volume:
120
Issue:
7
ISSN:
0027-8424
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Uncertainties about the magnitude of bycatch in poorly assessed fisheries impede effective conservation management. In northern Peru, small-scale fisheries (SSF) bycatch negatively impacts marine megafauna populations and the livelihoods of fishers which is further elevated by the under-reporting of incidents. Within the last decade, accounts of entangled humpback whales (HBW) ( Megaptera novaeangliae ) off the northern coast of Peru have increased, while Eastern Pacific leatherback turtles (LBT) ( Dermochelys coriacea ) have seen over a 90% decline in nesting populations related in large part to bycatch mortality. By leveraging the experience and knowledge of local fishers, our research objectives were to use a low-cost public participation mapping approach to provide a spatio-temporal assessment of bycatch risk for HBW and LBT off two Peruvian fishing ports. We used an open-source, geographic information systems (GIS) model, the Bycatch Risk Assessment (ByRA), as our platform. Broadly, ByRA identifies high bycatch risk areas by estimating the intersection of fishing areas (i.e., stressors) with species habitat and evaluating the exposure and consequence of possible interaction between the two. ByRA outputs provided risk maps and gear risk percentages categorized as high, medium, and low for the study area and seven subzones for HBW in the austral winter and LBT in the austral summer. Overall, the highest bycatch risk for both species was identified within gillnet fisheries near the coast. Bycatch risk for most gear types decreased with distance from the coast. When we separated the ByRA model by port, our map outputs indicate that bycatch management should be port specific, following seasonal and spatial variations for HBW, and specific fishing gear impacts for HBW and LBT. Combined with direct bycatch mitigation techniques, ByRA can be a supportive and informative tool for addressing specific bycatch threats and marine megafauna conservation goals. ByRA supports a participatory framework offering rapid visual information via risk maps and replicable methods for areas with limited resources and data on fisheries and species habitat. 
    more » « less
  2. Abstract

    To examine phylogenetic heterogeneity in turtle evolution, we collected thousands of high-confidence single-copy orthologs from 19 genome assemblies representative of extant turtle diversity and estimated a phylogeny with multispecies coalescent and concatenated partitioned methods. We also collected next-generation sequences from 26 turtle species and assembled millions of biallelic markers to reconstruct phylogenies based on annotated regions from the western painted turtle (Chrysemys picta bellii) genome (coding regions, introns, untranslated regions, intergenic, and others). We then measured gene tree-species tree discordance, as well as gene and site heterogeneity at each node in the inferred trees, and tested for temporal patterns in phylogenomic conflict across turtle evolution. We found strong and consistent support for all bifurcations in the inferred turtle species phylogenies. However, a number of genes, sites, and genomic features supported alternate relationships between turtle taxa. Our results suggest that gene tree-species tree discordance in these data sets is likely driven by population-level processes such as incomplete lineage sorting. We found very little effect of substitutional saturation on species tree topologies, and no clear phylogenetic patterns in codon usage bias and compositional heterogeneity. There was no correlation between gene and site concordance, node age, and DNA substitution rate across most annotated genomic regions. Our study demonstrates that heterogeneity is to be expected even in well-resolved clades such as turtles, and that future phylogenomic studies should aim to sample as much of the genome as possible in order to obtain accurate phylogenies for assessing conservation priorities in turtles. [Discordance; genomes; phylogeny; turtles.]

     
    more » « less
  3. Abstract

    A growing body of knowledge on the diversity and evolution of intertidal isopods across different regions worldwide has enhanced our understanding on biological diversification at the poorly studied, yet vast, sea–land interface. High genetic divergences among numerous allopatric lineages have been identified within presumed single broadly distributed species.Excirolana mayanais an intertidal isopod that is commonly found in sandy beaches throughout the Gulf of California. Its distribution in the Pacific extends from this basin to Colombia and in the Atlantic from Florida to Venezuela. Despite its broad distribution and ecological importance, its evolutionary history has been largely neglected. Herein, we examined phylogeographic patterns ofE. mayanain the Gulf of California and the Caribbean, based on maximum‐likelihood and Bayesian phylogenetic analyses ofDNAsequences from four mitochondrial genes (16SrDNA, 12SrDNA, cytochrome oxidase I gene, and cytochrome b gene). We compared the phylogeographic patterns ofE. mayanawith those of the coastal isopodsLigiaandExcirolana braziliensis(Gulf of California and Caribbean) andTylos(Gulf of California). We found highly divergent lineages in both, the Gulf of California and Caribbean, suggesting the presence of multiple species. We identified two instances of Atlantic–Pacific divergences. Some geographical structuring among the major clades found in the Caribbean is observed. Haplotypes from the Gulf of California form a monophyletic group sister to a lineage found in Venezuela. Phylogeographic patterns ofE. mayanain the Gulf of California differ from those observed inLigiaandTylosin this region. Nonetheless, several clades ofE. mayanahave similar distributions to clades of these two other isopod taxa. The high levels of cryptic diversity detected inE. mayanaalso pose challenges for the conservation of this isopod and its fragile environment, the sandy shores.

     
    more » « less
  4. Dinoflagellates of the family Symbiodiniaceae are crucial photosymbionts in corals and other marine organisms. Of these, Cladocopium goreaui is one of the most dominant symbiont species in the Indo-Pacific. Here, we present an improved genome assembly of C. goreaui combining new long-read sequence data with previously generated short-read data. Incorporating new full-length transcripts to guide gene prediction, the C. goreaui genome (1.2 Gb) exhibits a high extent of completeness (82.4% based on BUSCO protein recovery) and better resolution of repetitive sequence regions; 45,322 gene models were predicted, and 327 putative, topologically associated domains of the chromosomes were identified. Comparison with other Symbiodiniaceae genomes revealed a prevalence of repeats and duplicated genes in C. goreaui, and lineage-specific genes indicating functional innovation. Incorporating 2,841,408 protein sequences from 96 taxonomically diverse eukaryotes and representative prokaryotes in a phylogenomic approach, we assessed the evolutionary history of C. goreaui genes. Of the 5246 phylogenetic trees inferred from homologous protein sets containing two or more phyla, 35–36% have putatively originated via horizontal gene transfer (HGT), predominantly (19–23%) via an ancestral Archaeplastida lineage implicated in the endosymbiotic origin of plastids: 10–11% are of green algal origin, including genes encoding photosynthetic functions. Our results demonstrate the utility of long-read sequence data in resolving structural features of a dinoflagellate genome, and highlight how genetic transfer has shaped genome evolution of a facultative symbiont, and more broadly of dinoflagellates. 
    more » « less
  5. Xu, Jianping (Ed.)
    ABSTRACT Mitochondria originated from an ancient bacterial endosymbiont that underwent reductive evolution by gene loss and endosymbiont gene transfer to the nuclear genome. The diversity of mitochondrial genomes published to date has revealed that gene loss and transfer processes are ongoing in many lineages. Most well-studied eukaryotic lineages are represented in mitochondrial genome databases, except for the superphylum Retaria—the lineage comprising Foraminifera and Radiolaria. Using single-cell approaches, we determined two complete mitochondrial genomes of Foraminifera and two nearly complete mitochondrial genomes of radiolarians. We report the complete coding content of an additional 14 foram species. We show that foraminiferan and radiolarian mitochondrial genomes contain a nearly fully overlapping but reduced mitochondrial gene complement compared to other sequenced rhizarians. In contrast to animals and fungi, many protists encode a diverse set of proteins on their mitochondrial genomes, including several ribosomal genes; however, some aerobic eukaryotic lineages (euglenids, myzozoans, and chlamydomonas-like algae) have reduced mitochondrial gene content and lack all ribosomal genes. Similar to these reduced outliers, we show that retarian mitochondrial genomes lack ribosomal protein and tRNA genes, contain truncated and divergent small and large rRNA genes, and contain only 14 or 15 protein-coding genes, including nad1 , - 3 , - 4 , - 4L , - 5 , and - 7 , cob , cox1 , - 2 , and - 3 , and atp1 , - 6 , and - 9 , with forams and radiolarians additionally carrying nad2 and nad6 , respectively. In radiolarian mitogenomes, a noncanonical genetic code was identified in which all three stop codons encode amino acids. Collectively, these results add to our understanding of mitochondrial genome evolution and fill in one of the last major gaps in mitochondrial sequence databases. IMPORTANCE We present the reduced mitochondrial genomes of Retaria, the rhizarian lineage comprising the phyla Foraminifera and Radiolaria. By applying single-cell genomic approaches, we found that foraminiferan and radiolarian mitochondrial genomes contain an overlapping but reduced mitochondrial gene complement compared to other sequenced rhizarians. An alternative genetic code was identified in radiolarian mitogenomes in which all three stop codons encode amino acids. Collectively, these results shed light on the divergent nature of the mitochondrial genomes from an ecologically important group, warranting further questions into the biological underpinnings of gene content variability and genetic code variation between mitochondrial genomes. 
    more » « less