Relaxation of natural selection in the evolution of the giant lungfish genomes

Silvia Fuselli; Samuele Greco; Roberto Biello; Sergio Palmitessa; Marta Lago; Corrado Meneghetti; Carmel McDougall; Emiliano Trucchi; Omar Rota Stabelli; Assunta Maria Biscotti; Daniel J. Schmidt; David T. Roberts; Thomas Espinoza; Jane Margaret Hughes; Lino Ometto; Marco Gerdol; Giorgio Bertorelle

doi:10.1093/molbev/msad193

Relaxation of natural selection in the evolution of the giant lungfish genomes

Silvia Fuselli^*, Samuele Greco, Roberto Biello, Sergio Palmitessa, Marta Lago, Corrado Meneghetti, Carmel McDougall, Emiliano Trucchi, Omar Rota Stabelli, Assunta Maria Biscotti, Daniel J. Schmidt, David T. Roberts, Thomas Espinoza, Jane Margaret Hughes, Lino Ometto, Marco Gerdol, Giorgio Bertorelle^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

Abstract

Nonadaptive hypotheses on the evolution of eukaryotic genome size predict an expansion when the process of purifying selection becomes weak. Accordingly, species with huge genomes, such as lungfish, are expected to show a genome-wide relaxation signature of selection compared with other organisms. However, few studies have empirically tested this prediction using genomic data in a comparative framework. Here, we show that 1) the newly assembled transcriptome of the Australian lungfish, Neoceratodus forsteri, is characterized by an excess of pervasive transcription, or transcriptional leakage, possibly due to suboptimal transcriptional control, and 2) a significant relaxation signature in coding genes in lungfish species compared with other vertebrates. Based on these observations, we propose that the largest known animal genomes evolved in a nearly neutral scenario where genome expansion is less efficiently constrained.

Original language	English
Article number	msad193
Pages (from-to)	1-6
Number of pages	6
Journal	Molecular Biology and Evolution
Volume	40
Issue number	9
Early online date	6 Sept 2023
DOIs	https://doi.org/10.1093/molbev/msad193
Publication status	Published - Sept 2023

Keywords

Australian lungfish (Neoceratodus forsteri)
Genome size evolution
Lungfish
Pervasive transcription
Relaxation of natural selection

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10.1093/molbev/msad193Licence: CC BY

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Fuselli, S., Greco, S., Biello, R., Palmitessa, S., Lago, M., Meneghetti, C., McDougall, C., Trucchi, E., Rota Stabelli, O., Biscotti, A. M., Schmidt, D. J., Roberts, D. T., Espinoza, T., Hughes, J. M., Ometto, L., Gerdol, M., & Bertorelle, G. (2023). Relaxation of natural selection in the evolution of the giant lungfish genomes. Molecular Biology and Evolution, 40(9), 1-6. Article msad193. https://doi.org/10.1093/molbev/msad193

@article{d27f4b8132f147ecb691bf420159010d,

title = "Relaxation of natural selection in the evolution of the giant lungfish genomes",

abstract = "Nonadaptive hypotheses on the evolution of eukaryotic genome size predict an expansion when the process of purifying selection becomes weak. Accordingly, species with huge genomes, such as lungfish, are expected to show a genome-wide relaxation signature of selection compared with other organisms. However, few studies have empirically tested this prediction using genomic data in a comparative framework. Here, we show that 1) the newly assembled transcriptome of the Australian lungfish, Neoceratodus forsteri, is characterized by an excess of pervasive transcription, or transcriptional leakage, possibly due to suboptimal transcriptional control, and 2) a significant relaxation signature in coding genes in lungfish species compared with other vertebrates. Based on these observations, we propose that the largest known animal genomes evolved in a nearly neutral scenario where genome expansion is less efficiently constrained.",

keywords = "Australian lungfish (Neoceratodus forsteri), Genome size evolution, Lungfish, Pervasive transcription, Relaxation of natural selection",

author = "Silvia Fuselli and Samuele Greco and Roberto Biello and Sergio Palmitessa and Marta Lago and Corrado Meneghetti and Carmel McDougall and Emiliano Trucchi and {Rota Stabelli}, Omar and Biscotti, {Assunta Maria} and Schmidt, {Daniel J.} and Roberts, {David T.} and Thomas Espinoza and Hughes, {Jane Margaret} and Lino Ometto and Marco Gerdol and Giorgio Bertorelle",

note = "Funding: This work was supported by the University of Ferrara (Italy) and funded by the MIUR PRIN 2017 grant 201794ZXTL to G.B. S.F., G.B., and R.B. are deeply grateful to Jane Hughes and Dan Schmidt for their hospitality at the Griffith University, Queensland, and for their friendship.",

year = "2023",

month = sep,

doi = "10.1093/molbev/msad193",

language = "English",

volume = "40",

pages = "1--6",

journal = "Molecular Biology and Evolution",

issn = "0737-4038",

publisher = "Oxford University Press",

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Fuselli, S, Greco, S, Biello, R, Palmitessa, S, Lago, M, Meneghetti, C, McDougall, C, Trucchi, E, Rota Stabelli, O, Biscotti, AM, Schmidt, DJ, Roberts, DT, Espinoza, T, Hughes, JM, Ometto, L, Gerdol, M & Bertorelle, G 2023, 'Relaxation of natural selection in the evolution of the giant lungfish genomes', Molecular Biology and Evolution, vol. 40, no. 9, msad193, pp. 1-6. https://doi.org/10.1093/molbev/msad193

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T1 - Relaxation of natural selection in the evolution of the giant lungfish genomes

AU - Fuselli, Silvia

AU - Greco, Samuele

AU - Biello, Roberto

AU - Palmitessa, Sergio

AU - Lago, Marta

AU - Meneghetti, Corrado

AU - McDougall, Carmel

AU - Trucchi, Emiliano

AU - Rota Stabelli, Omar

AU - Biscotti, Assunta Maria

AU - Schmidt, Daniel J.

AU - Roberts, David T.

AU - Espinoza, Thomas

AU - Hughes, Jane Margaret

AU - Ometto, Lino

AU - Gerdol, Marco

AU - Bertorelle, Giorgio

N1 - Funding: This work was supported by the University of Ferrara (Italy) and funded by the MIUR PRIN 2017 grant 201794ZXTL to G.B. S.F., G.B., and R.B. are deeply grateful to Jane Hughes and Dan Schmidt for their hospitality at the Griffith University, Queensland, and for their friendship.

PY - 2023/9

Y1 - 2023/9

N2 - Nonadaptive hypotheses on the evolution of eukaryotic genome size predict an expansion when the process of purifying selection becomes weak. Accordingly, species with huge genomes, such as lungfish, are expected to show a genome-wide relaxation signature of selection compared with other organisms. However, few studies have empirically tested this prediction using genomic data in a comparative framework. Here, we show that 1) the newly assembled transcriptome of the Australian lungfish, Neoceratodus forsteri, is characterized by an excess of pervasive transcription, or transcriptional leakage, possibly due to suboptimal transcriptional control, and 2) a significant relaxation signature in coding genes in lungfish species compared with other vertebrates. Based on these observations, we propose that the largest known animal genomes evolved in a nearly neutral scenario where genome expansion is less efficiently constrained.

AB - Nonadaptive hypotheses on the evolution of eukaryotic genome size predict an expansion when the process of purifying selection becomes weak. Accordingly, species with huge genomes, such as lungfish, are expected to show a genome-wide relaxation signature of selection compared with other organisms. However, few studies have empirically tested this prediction using genomic data in a comparative framework. Here, we show that 1) the newly assembled transcriptome of the Australian lungfish, Neoceratodus forsteri, is characterized by an excess of pervasive transcription, or transcriptional leakage, possibly due to suboptimal transcriptional control, and 2) a significant relaxation signature in coding genes in lungfish species compared with other vertebrates. Based on these observations, we propose that the largest known animal genomes evolved in a nearly neutral scenario where genome expansion is less efficiently constrained.

KW - Australian lungfish (Neoceratodus forsteri)

KW - Genome size evolution

KW - Lungfish

KW - Pervasive transcription

KW - Relaxation of natural selection

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DO - 10.1093/molbev/msad193

M3 - Article

C2 - 37671664

AN - SCOPUS:85171600819

SN - 0737-4038

VL - 40

SP - 1

EP - 6

JO - Molecular Biology and Evolution

JF - Molecular Biology and Evolution

IS - 9

M1 - msad193

ER -

Relaxation of natural selection in the evolution of the giant lungfish genomes

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