Nuclear environmental DNA resolves fine-scale population genetic structure in an aquatic habitat

Zifang Liu; Mary A. Kishe; Nestory P. Gabagambi; Asilatu H. Shechonge; Benjamin P. Ngatunga; Katie Smith; Andrew D. Saxon; Alan G. Hudson; Tyler Linderoth; George F. Turner; Rupert A. Collins; Martin J. Genner

doi:10.1016/j.isci.2023.108669

Nuclear environmental DNA resolves fine-scale population genetic structure in an aquatic habitat

Zifang Liu, Mary A. Kishe, Nestory P. Gabagambi, Asilatu H. Shechonge, Benjamin P. Ngatunga, Katie Smith, Andrew D. Saxon, Alan G. Hudson, Tyler Linderoth, George F. Turner, Rupert A. Collins, Martin J. Genner^*

^*Corresponding author for this work

Research output: Contribution to journal › Article (Academic Journal) › peer-review

4 Citations (Scopus)

Abstract

There is considerable potential for nuclear genomic material in environmental DNA (eDNA) to inform us of population genetic structure within aquatic species. We tested if nuclear allelic composition data sourced from eDNA can resolve fine scale spatial genetic structure of the cichlid fish Astatotilapia calliptera in Lake Masoko, Tanzania. In this ∼35 m deep crater lake the species is diverging into two genetically distinguishable ecomorphs, separated by a thermo-oxycline at ∼15 m that divides biologically distinct water masses. We quantified population genetic structure along a depth transect using single nucleotide polymorphisms (SNPs) derived from genome sequencing of 530 individuals. This population genetic structure was reflected in a focal set of SNPs that were also reliably amplified from eDNA — with allele frequencies derived from eDNA reflecting those of fish within each depth zone. Thus, by targeting known genetic variation between populations within aquatic eDNA, we measured genetic structure within the focal species.

Original language	English
Article number	108669
Journal	iScience
Volume	27
Issue number	1
Early online date	22 Dec 2023
DOIs	https://doi.org/10.1016/j.isci.2023.108669
Publication status	Published - 19 Jan 2024

Bibliographical note

Funding Information:
We thank staff of the Tanzania Fisheries Research Institute for support during fieldwork. We thank the researchers who contributed to the collection of fish and generation and analysis of whole genome data from Lake Masoko Astatotilapia calliptera, including Emília Santos, Grégoire Vernaz, Richard Durbin, Eric Miska, and Hannah Munby. We thank Julie Johnson for fish paintings. M.J.G. and G.F.T. were supported by NERC award NE/S001794/1 . Z.L. was supported by a studentship from the China Scholarship Council . We thank Christy Waterfall and Jane Coghill from the University of Bristol Genomics Facility for sequencing support.

Funding Information:
We thank staff of the Tanzania Fisheries Research Institute for support during fieldwork. We thank the researchers who contributed to the collection of fish and generation and analysis of whole genome data from Lake Masoko Astatotilapia calliptera, including Emília Santos, Grégoire Vernaz, Richard Durbin, Eric Miska, and Hannah Munby. We thank Julie Johnson for fish paintings. M.J.G. and G.F.T. were supported by NERC award NE/S001794/1. Z.L. was supported by a studentship from the China Scholarship Council. We thank Christy Waterfall and Jane Coghill from the University of Bristol Genomics Facility for sequencing support. Conceptualization, R.A.C. and M.J.G. Data curation Z.L. R.A.C. and M.J.G. Formal Analysis, Z.L. R.A.C. and M.J.G. Funding Acquisition, Z.L. G.F.T. and M.J.G. Investigation, Z.L. M.A.K. P.N.G. K.S. A.D.S. R.A.C. A.G.H. and M.J.G. Methodology, Z.L. R.A.C. and M.J.G. Project administration, M.A.K. A.H.S. and M.J.G. Resources, A.H. T.L. G.F.T. and M.J.G. Supervision, R.A.C. and M.J.G. Visualization, Z.L. R.A.C. and M.J.G. Writing – original draft, Z.L. R.A.C. and M.J.G. Writing – review and editing, All authors. The authors have no competing interests to declare.

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© 2023 The Authors

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@article{d90a4519fdf542f3ba88ad5e56127f86,

title = "Nuclear environmental DNA resolves fine-scale population genetic structure in an aquatic habitat",

abstract = "There is considerable potential for nuclear genomic material in environmental DNA (eDNA) to inform us of population genetic structure within aquatic species. We tested if nuclear allelic composition data sourced from eDNA can resolve fine scale spatial genetic structure of the cichlid fish Astatotilapia calliptera in Lake Masoko, Tanzania. In this ∼35 m deep crater lake the species is diverging into two genetically distinguishable ecomorphs, separated by a thermo-oxycline at ∼15 m that divides biologically distinct water masses. We quantified population genetic structure along a depth transect using single nucleotide polymorphisms (SNPs) derived from genome sequencing of 530 individuals. This population genetic structure was reflected in a focal set of SNPs that were also reliably amplified from eDNA — with allele frequencies derived from eDNA reflecting those of fish within each depth zone. Thus, by targeting known genetic variation between populations within aquatic eDNA, we measured genetic structure within the focal species.",

author = "Zifang Liu and Kishe, {Mary A.} and Gabagambi, {Nestory P.} and Shechonge, {Asilatu H.} and Ngatunga, {Benjamin P.} and Katie Smith and Saxon, {Andrew D.} and Hudson, {Alan G.} and Tyler Linderoth and Turner, {George F.} and Collins, {Rupert A.} and Genner, {Martin J.}",

note = "Funding Information: We thank staff of the Tanzania Fisheries Research Institute for support during fieldwork. We thank the researchers who contributed to the collection of fish and generation and analysis of whole genome data from Lake Masoko Astatotilapia calliptera, including Em{\'i}lia Santos, Gr{\'e}goire Vernaz, Richard Durbin, Eric Miska, and Hannah Munby. We thank Julie Johnson for fish paintings. M.J.G. and G.F.T. were supported by NERC award NE/S001794/1 . Z.L. was supported by a studentship from the China Scholarship Council . We thank Christy Waterfall and Jane Coghill from the University of Bristol Genomics Facility for sequencing support. Funding Information: We thank staff of the Tanzania Fisheries Research Institute for support during fieldwork. We thank the researchers who contributed to the collection of fish and generation and analysis of whole genome data from Lake Masoko Astatotilapia calliptera, including Em{\'i}lia Santos, Gr{\'e}goire Vernaz, Richard Durbin, Eric Miska, and Hannah Munby. We thank Julie Johnson for fish paintings. M.J.G. and G.F.T. were supported by NERC award NE/S001794/1. Z.L. was supported by a studentship from the China Scholarship Council. We thank Christy Waterfall and Jane Coghill from the University of Bristol Genomics Facility for sequencing support. Conceptualization, R.A.C. and M.J.G. Data curation Z.L. R.A.C. and M.J.G. Formal Analysis, Z.L. R.A.C. and M.J.G. Funding Acquisition, Z.L. G.F.T. and M.J.G. Investigation, Z.L. M.A.K. P.N.G. K.S. A.D.S. R.A.C. A.G.H. and M.J.G. Methodology, Z.L. R.A.C. and M.J.G. Project administration, M.A.K. A.H.S. and M.J.G. Resources, A.H. T.L. G.F.T. and M.J.G. Supervision, R.A.C. and M.J.G. Visualization, Z.L. R.A.C. and M.J.G. Writing – original draft, Z.L. R.A.C. and M.J.G. Writing – review and editing, All authors. The authors have no competing interests to declare. Publisher Copyright: {\textcopyright} 2023 The Authors",

year = "2024",

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doi = "10.1016/j.isci.2023.108669",

language = "English",

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T1 - Nuclear environmental DNA resolves fine-scale population genetic structure in an aquatic habitat

AU - Liu, Zifang

AU - Kishe, Mary A.

AU - Gabagambi, Nestory P.

AU - Shechonge, Asilatu H.

AU - Ngatunga, Benjamin P.

AU - Smith, Katie

AU - Saxon, Andrew D.

AU - Hudson, Alan G.

AU - Linderoth, Tyler

AU - Turner, George F.

AU - Collins, Rupert A.

AU - Genner, Martin J.

N1 - Funding Information: We thank staff of the Tanzania Fisheries Research Institute for support during fieldwork. We thank the researchers who contributed to the collection of fish and generation and analysis of whole genome data from Lake Masoko Astatotilapia calliptera, including Emília Santos, Grégoire Vernaz, Richard Durbin, Eric Miska, and Hannah Munby. We thank Julie Johnson for fish paintings. M.J.G. and G.F.T. were supported by NERC award NE/S001794/1 . Z.L. was supported by a studentship from the China Scholarship Council . We thank Christy Waterfall and Jane Coghill from the University of Bristol Genomics Facility for sequencing support. Funding Information: We thank staff of the Tanzania Fisheries Research Institute for support during fieldwork. We thank the researchers who contributed to the collection of fish and generation and analysis of whole genome data from Lake Masoko Astatotilapia calliptera, including Emília Santos, Grégoire Vernaz, Richard Durbin, Eric Miska, and Hannah Munby. We thank Julie Johnson for fish paintings. M.J.G. and G.F.T. were supported by NERC award NE/S001794/1. Z.L. was supported by a studentship from the China Scholarship Council. We thank Christy Waterfall and Jane Coghill from the University of Bristol Genomics Facility for sequencing support. Conceptualization, R.A.C. and M.J.G. Data curation Z.L. R.A.C. and M.J.G. Formal Analysis, Z.L. R.A.C. and M.J.G. Funding Acquisition, Z.L. G.F.T. and M.J.G. Investigation, Z.L. M.A.K. P.N.G. K.S. A.D.S. R.A.C. A.G.H. and M.J.G. Methodology, Z.L. R.A.C. and M.J.G. Project administration, M.A.K. A.H.S. and M.J.G. Resources, A.H. T.L. G.F.T. and M.J.G. Supervision, R.A.C. and M.J.G. Visualization, Z.L. R.A.C. and M.J.G. Writing – original draft, Z.L. R.A.C. and M.J.G. Writing – review and editing, All authors. The authors have no competing interests to declare. Publisher Copyright: © 2023 The Authors

PY - 2024/1/19

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N2 - There is considerable potential for nuclear genomic material in environmental DNA (eDNA) to inform us of population genetic structure within aquatic species. We tested if nuclear allelic composition data sourced from eDNA can resolve fine scale spatial genetic structure of the cichlid fish Astatotilapia calliptera in Lake Masoko, Tanzania. In this ∼35 m deep crater lake the species is diverging into two genetically distinguishable ecomorphs, separated by a thermo-oxycline at ∼15 m that divides biologically distinct water masses. We quantified population genetic structure along a depth transect using single nucleotide polymorphisms (SNPs) derived from genome sequencing of 530 individuals. This population genetic structure was reflected in a focal set of SNPs that were also reliably amplified from eDNA — with allele frequencies derived from eDNA reflecting those of fish within each depth zone. Thus, by targeting known genetic variation between populations within aquatic eDNA, we measured genetic structure within the focal species.

AB - There is considerable potential for nuclear genomic material in environmental DNA (eDNA) to inform us of population genetic structure within aquatic species. We tested if nuclear allelic composition data sourced from eDNA can resolve fine scale spatial genetic structure of the cichlid fish Astatotilapia calliptera in Lake Masoko, Tanzania. In this ∼35 m deep crater lake the species is diverging into two genetically distinguishable ecomorphs, separated by a thermo-oxycline at ∼15 m that divides biologically distinct water masses. We quantified population genetic structure along a depth transect using single nucleotide polymorphisms (SNPs) derived from genome sequencing of 530 individuals. This population genetic structure was reflected in a focal set of SNPs that were also reliably amplified from eDNA — with allele frequencies derived from eDNA reflecting those of fish within each depth zone. Thus, by targeting known genetic variation between populations within aquatic eDNA, we measured genetic structure within the focal species.

U2 - 10.1016/j.isci.2023.108669

DO - 10.1016/j.isci.2023.108669

M3 - Article (Academic Journal)

C2 - 38226161

SN - 2589-0042

VL - 27

JO - iScience

JF - iScience

IS - 1

M1 - 108669

ER -

Nuclear environmental DNA resolves fine-scale population genetic structure in an aquatic habitat

Abstract

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