Parental microbiota modulates offspring development, body mass and fecundity in a polyphagous fruit fly

Binh Nguyen; Anh Than; Hue Dinh; Juliano Morimoto; Fleur Ponton

doi:10.3390/microorganisms8091289

Parental microbiota modulates offspring development, body mass and fecundity in a polyphagous fruit fly

Binh Nguyen, Anh Than, Hue Dinh, Juliano Morimoto, Fleur Ponton^*

^*Corresponding author for this work

Aberdeen Centre For Environmental Sustainability

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

7 Citations (Scopus)

2 Downloads (Pure)

Abstract

The commensal microbiota is a key modulator of animal fitness, but little is known about the extent to which the parental microbiota influences fitness-related traits of future generations. We addressed this gap by manipulating the parental microbiota of a polyphagous fruit fly (Bactrocera tryoni) and measuring offspring developmental traits, body composition, and fecundity. We generated three parental microbiota treatments where parents had a microbiota that was non-manipulated (control), removed (axenic), or removed-and-reintroduced (reinoculation). We found that the percentage of egg hatching, of pupal production, and body weight of larvae and adult females were lower in offspring of axenic parents compared to that of non-axenic parents. The percentage of partially emerged adults was higher, and fecundity of adult females was lower in offspring of axenic parents relative to offspring of control and reinoculated parents. There was no significant effect of parental microbiota manipulation on offspring developmental time or lipid reserve. Our results reveal transgenerational effects of the parental commensal microbiota on different aspects of offspring life-history traits, thereby providing a better understanding of the long-lasting effects of host–microbe interactions.

Original language	English
Article number	1289
Pages (from-to)	1-11
Number of pages	11
Journal	Microorganisms
Volume	8
Issue number	9
DOIs	https://doi.org/10.3390/microorganisms8091289
Publication status	Published - 24 Aug 2020

Bibliographical note

Funding Information:
Funding: Project Raising Q-fly Sterile Insect Technique to World Standard (HG14033) is funded by the Hort Frontiers Fruit Fly Fund, part of the Hort Frontiers strategic partnership initiative developed by Hort Innovation, with co-investment from Macquarie University (NSW, Australia) and contributions from the Australian Government. BN is funded by the international Research Training Program (iRTP) scholarship from Macquarie University and the Australian Government. HD was supported by Macquarie University Research Excellence Scholarship and AT was supported by MQ-VIED Joint Scholarship.

Publisher Copyright:
© 2020 by the authors. Licensee MDPI, Basel, Switzerland.

Keywords

Gut microbiota
Life-history traits
Offspring performance
Reproductive success
Transgenerational effects

Access to Document

10.3390/microorganisms8091289

Nguyen_etal_Parental_Microbiota_Modulates_VOR
This is an open access article distributed under the Creative Commons Attribution License which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Final published version, 651 KBLicence: CC BY

Cite this

@article{b3b77996cf4b48f08dcc7dadebbd1c9c,

title = "Parental microbiota modulates offspring development, body mass and fecundity in a polyphagous fruit fly",

abstract = "The commensal microbiota is a key modulator of animal fitness, but little is known about the extent to which the parental microbiota influences fitness-related traits of future generations. We addressed this gap by manipulating the parental microbiota of a polyphagous fruit fly (Bactrocera tryoni) and measuring offspring developmental traits, body composition, and fecundity. We generated three parental microbiota treatments where parents had a microbiota that was non-manipulated (control), removed (axenic), or removed-and-reintroduced (reinoculation). We found that the percentage of egg hatching, of pupal production, and body weight of larvae and adult females were lower in offspring of axenic parents compared to that of non-axenic parents. The percentage of partially emerged adults was higher, and fecundity of adult females was lower in offspring of axenic parents relative to offspring of control and reinoculated parents. There was no significant effect of parental microbiota manipulation on offspring developmental time or lipid reserve. Our results reveal transgenerational effects of the parental commensal microbiota on different aspects of offspring life-history traits, thereby providing a better understanding of the long-lasting effects of host–microbe interactions.",

keywords = "Gut microbiota, Life-history traits, Offspring performance, Reproductive success, Transgenerational effects",

author = "Binh Nguyen and Anh Than and Hue Dinh and Juliano Morimoto and Fleur Ponton",

note = "Funding Information: Funding: Project Raising Q-fly Sterile Insect Technique to World Standard (HG14033) is funded by the Hort Frontiers Fruit Fly Fund, part of the Hort Frontiers strategic partnership initiative developed by Hort Innovation, with co-investment from Macquarie University (NSW, Australia) and contributions from the Australian Government. BN is funded by the international Research Training Program (iRTP) scholarship from Macquarie University and the Australian Government. HD was supported by Macquarie University Research Excellence Scholarship and AT was supported by MQ-VIED Joint Scholarship. Publisher Copyright: {\textcopyright} 2020 by the authors. Licensee MDPI, Basel, Switzerland.",

year = "2020",

month = aug,

day = "24",

doi = "10.3390/microorganisms8091289",

language = "English",

volume = "8",

pages = "1--11",

journal = "Microorganisms",

issn = "2076-2607",

publisher = "MDPI AG",

number = "9",

}

TY - JOUR

T1 - Parental microbiota modulates offspring development, body mass and fecundity in a polyphagous fruit fly

AU - Nguyen, Binh

AU - Than, Anh

AU - Dinh, Hue

AU - Morimoto, Juliano

AU - Ponton, Fleur

N1 - Funding Information: Funding: Project Raising Q-fly Sterile Insect Technique to World Standard (HG14033) is funded by the Hort Frontiers Fruit Fly Fund, part of the Hort Frontiers strategic partnership initiative developed by Hort Innovation, with co-investment from Macquarie University (NSW, Australia) and contributions from the Australian Government. BN is funded by the international Research Training Program (iRTP) scholarship from Macquarie University and the Australian Government. HD was supported by Macquarie University Research Excellence Scholarship and AT was supported by MQ-VIED Joint Scholarship. Publisher Copyright: © 2020 by the authors. Licensee MDPI, Basel, Switzerland.

PY - 2020/8/24

Y1 - 2020/8/24

N2 - The commensal microbiota is a key modulator of animal fitness, but little is known about the extent to which the parental microbiota influences fitness-related traits of future generations. We addressed this gap by manipulating the parental microbiota of a polyphagous fruit fly (Bactrocera tryoni) and measuring offspring developmental traits, body composition, and fecundity. We generated three parental microbiota treatments where parents had a microbiota that was non-manipulated (control), removed (axenic), or removed-and-reintroduced (reinoculation). We found that the percentage of egg hatching, of pupal production, and body weight of larvae and adult females were lower in offspring of axenic parents compared to that of non-axenic parents. The percentage of partially emerged adults was higher, and fecundity of adult females was lower in offspring of axenic parents relative to offspring of control and reinoculated parents. There was no significant effect of parental microbiota manipulation on offspring developmental time or lipid reserve. Our results reveal transgenerational effects of the parental commensal microbiota on different aspects of offspring life-history traits, thereby providing a better understanding of the long-lasting effects of host–microbe interactions.

AB - The commensal microbiota is a key modulator of animal fitness, but little is known about the extent to which the parental microbiota influences fitness-related traits of future generations. We addressed this gap by manipulating the parental microbiota of a polyphagous fruit fly (Bactrocera tryoni) and measuring offspring developmental traits, body composition, and fecundity. We generated three parental microbiota treatments where parents had a microbiota that was non-manipulated (control), removed (axenic), or removed-and-reintroduced (reinoculation). We found that the percentage of egg hatching, of pupal production, and body weight of larvae and adult females were lower in offspring of axenic parents compared to that of non-axenic parents. The percentage of partially emerged adults was higher, and fecundity of adult females was lower in offspring of axenic parents relative to offspring of control and reinoculated parents. There was no significant effect of parental microbiota manipulation on offspring developmental time or lipid reserve. Our results reveal transgenerational effects of the parental commensal microbiota on different aspects of offspring life-history traits, thereby providing a better understanding of the long-lasting effects of host–microbe interactions.

KW - Gut microbiota

KW - Life-history traits

KW - Offspring performance

KW - Reproductive success

KW - Transgenerational effects

UR - http://www.scopus.com/inward/record.url?scp=85090607387&partnerID=8YFLogxK

U2 - 10.3390/microorganisms8091289

DO - 10.3390/microorganisms8091289

M3 - Article

C2 - 32846933

AN - SCOPUS:85090607387

SN - 2076-2607

VL - 8

SP - 1

EP - 11

JO - Microorganisms

JF - Microorganisms

IS - 9

M1 - 1289

ER -

Parental microbiota modulates offspring development, body mass and fecundity in a polyphagous fruit fly

Abstract

Bibliographical note

Keywords

Access to Document

Other files and links

Fingerprint

Cite this