Rapid genomic expansion and purging associated with habitat transitions in a clade of beach crustaceans (Haustoriidae: Amphipoda)

Abstract

Genome sizes vary by orders of magnitude across the Tree of Life and lack any correlation with organismal complexity. Some crustacean orders, such as amphipods, have genome sizes that correlate with body size, temperature, and water depth, indicating that natural selection may constrain genome sizes due to physiological pressures. In this study, we examine the relationship between genome size, repetitive content, and environmental variables on a clade of sand-burrowing amphipods (Haustoriidae) that are distributed across the Gulf of Mexico and the North Atlantic. We uncover a 6-fold genome size variation within a clade that is less than 7 million years old. Unlike previous studies, we find no correlation between genome size and latitude, but do uncover a significant relationship between genome size and body length. Further, we find that the proportion of repetitive content predicts genome size, and that the largest genomes appear to be driven by expansions of LINE elements. Finally, we find evidence of genomic purging and body size reduction in two lineages that have independently colonized warm brackish waters, possibly indicating a strong physiological constraint of transitioning from surf-swept beaches to protected bays.Significance StatementThe evolution of genome size has been a long-standing puzzle in biology. In this work, we find that genome sizes may be driven by different selection regimes following shifts to a new habitat. Dramatic genome size changes can occur rapidly, in only a few million years.Data Availability StatementRaw data sheets have been deposited on Dryad: SUBMITTED. Raw sequence reads are available at from NCBI under Bioproject SUBMITTED.

Origin and evolution of the Haustoriidae (Amphipoda): a eulogy for the Haustoriidira

“…Infraorder Lysianassida Dana, 1849Parvorder Haustoriidira Stebbing, 1906Superfamily Haustorioidea Stebbing, 1906 Family Cheidae Thurston, 1982 Family Condukiidae Barnard & Drummond, 1982 SAMPLE COLLECTION Samples from the United States were collected using methods in Hancock et al (2020) and were preserved in 95% ethanol. Eohaustorius estuarius from the Pacific coast was collected by Gary Buhler of Northwest Amphipod, LLC.…”

“…In addition to samples collected specifically for this study, we incorporated datasets from three studies: Hancock et al (2019), Hancock et al (2020), andCopilaş-Ciocianu et al (2020).…”

“…This study found support for widespread cryptic diversity among haustoriid species, and a range of species delimitation techniques identified at least 4 independent lineages within the nominal species L. triarticulatus. Hancock et al (2020) followed this work by expanding sampling to haustoriid species endemic to the North Atlantic and the Pacific. However, this work focused specifically on the evolution of genome size within the family and did not comment on the specific relationships inferred.…”

Origin and evolution of the Haustoriidae (Amphipoda): A eulogy for the Haustoriidira

“…Samples from the United States were collected using methods in Hancock et al (2020) and were preserved in 95% ethanol. Eohaustorius estuarius from the Pacific coast was collected by Gary Buhler of Northwest Amphipod, LLC.…”

“…To estimate the age of the Haustoriidae, we used BEAST2 on the full concatenated dataset (n = 95) and applied 5 calibration points from Copilaş-Ciocianu et al (2020) and Hancock et al 2020. Age ranges to follow represent the 95% highest posterior density (HPD).…”