M E Bunker1, G Elliott1, H Heyer-Gray1, M O Martin1, A E Arnold2, S L Weiss3. 1. Department of Biology, University of Puget Sound, Tacoma, WA, USA. 2. School of Plant Sciences and Department of Ecology and Evolutionary Biology, University of Arizona, AZ, Tucson, USA. 3. Department of Biology, University of Puget Sound, Tacoma, WA, USA. sweiss@pugetsound.edu.
Abstract
BACKGROUND: Beneficial microbes can be vertically transmitted from mother to offspring in many organisms. In oviparous animals, bacterial transfer to eggs may improve egg success by inhibiting fungal attachment and infection from pathogenic microbes in the nest environment. Vertical transfer of these egg-protective bacteria may be facilitated through behavioral mechanisms such as egg-tending, but many species do not provide parental care. Thus, an important mechanism of vertical transfer may be the passage of the egg through the maternal cloaca during oviposition itself. In this study, we examined how oviposition affects eggshell microbial communities, fungal attachment, hatch success, and offspring phenotype in the striped plateau lizard, Sceloporus virgatus, a species with no post-oviposition parental care. RESULTS: Relative to dissected eggs that did not pass through the cloaca, oviposited eggs had more bacteria and fewer fungal hyphae when examined with a scanning electron microscope. Using high throughput Illumina sequencing, we also found a difference in the bacterial communities of eggshells that did and did not pass through the cloaca, and the diversity of eggshell communities tended to correlate with maternal cloacal diversity only for oviposited eggs, and not for dissected eggs, indicating that vertical transmission of microbes is occurring. Further, we found that oviposited eggs had greater hatch success and led to larger offspring than those that were dissected. CONCLUSIONS: Overall, our results indicate that female S. virgatus lizards transfer beneficial microbes from their cloaca onto their eggs during oviposition, and that these microbes reduce fungal colonization and infection of eggs during incubation and increase female fitness. Cloacal transfer of egg-protective bacteria may be common among oviparous species, and may be especially advantageous to species that lack parental care.
BACKGROUND: Beneficial microbes can be vertically transmitted from mother to offspring in many organisms. In oviparous animals, bacterial transfer to eggs may improve egg success by inhibiting fungal attachment and infection from pathogenic microbes in the nest environment. Vertical transfer of these egg-protective bacteria may be facilitated through behavioral mechanisms such as egg-tending, but many species do not provide parental care. Thus, an important mechanism of vertical transfer may be the passage of the egg through the maternal cloaca during oviposition itself. In this study, we examined how oviposition affects eggshell microbial communities, fungal attachment, hatch success, and offspring phenotype in the striped plateau lizard, Sceloporus virgatus, a species with no post-oviposition parental care. RESULTS: Relative to dissected eggs that did not pass through the cloaca, oviposited eggs had more bacteria and fewer fungal hyphae when examined with a scanning electron microscope. Using high throughput Illumina sequencing, we also found a difference in the bacterial communities of eggshells that did and did not pass through the cloaca, and the diversity of eggshell communities tended to correlate with maternal cloacal diversity only for oviposited eggs, and not for dissected eggs, indicating that vertical transmission of microbes is occurring. Further, we found that oviposited eggs had greater hatch success and led to larger offspring than those that were dissected. CONCLUSIONS: Overall, our results indicate that female S. virgatus lizards transfer beneficial microbes from their cloaca onto their eggs during oviposition, and that these microbes reduce fungal colonization and infection of eggs during incubation and increase female fitness. Cloacal transfer of egg-protective bacteria may be common among oviparous species, and may be especially advantageous to species that lack parental care.
Authors: Kevin D Kohl; Antonio Brun; Melisa Magallanes; Joshua Brinkerhoff; Alejandro Laspiur; Juan Carlos Acosta; Enrique Caviedes-Vidal; Seth R Bordenstein Journal: Mol Ecol Date: 2016-12-14 Impact factor: 6.185
Authors: Margaret McFall-Ngai; Michael G Hadfield; Thomas C G Bosch; Hannah V Carey; Tomislav Domazet-Lošo; Angela E Douglas; Nicole Dubilier; Gerard Eberl; Tadashi Fukami; Scott F Gilbert; Ute Hentschel; Nicole King; Staffan Kjelleberg; Andrew H Knoll; Natacha Kremer; Sarkis K Mazmanian; Jessica L Metcalf; Kenneth Nealson; Naomi E Pierce; John F Rawls; Ann Reid; Edward G Ruby; Mary Rumpho; Jon G Sanders; Diethard Tautz; Jennifer J Wernegreen Journal: Proc Natl Acad Sci U S A Date: 2013-02-07 Impact factor: 11.205
Authors: Jana M U'Ren; François Lutzoni; Jolanta Miadlikowska; Naupaka B Zimmerman; Ignazio Carbone; Georgiana May; A Elizabeth Arnold Journal: Nat Ecol Evol Date: 2019-09-23 Impact factor: 15.460
Authors: Michael J Taylor; R William Mannan; Jana M U'Ren; Nicholas P Garber; Rachel E Gallery; A Elizabeth Arnold Journal: BMC Microbiol Date: 2019-02-21 Impact factor: 3.605
Authors: Rebekka S Janke; Filip Kaftan; Sarah P Niehs; Kirstin Scherlach; Andre Rodrigues; Aleš Svatoš; Christian Hertweck; Martin Kaltenpoth; Laura V Flórez Journal: ISME J Date: 2022-09-02 Impact factor: 11.217
Authors: Garima Kulshreshtha; Liliana D'Alba; Ian C Dunn; Sophie Rehault-Godbert; Alejandro B Rodriguez-Navarro; Maxwell T Hincke Journal: Front Immunol Date: 2022-02-25 Impact factor: 7.561
Authors: Muhammad Riaz; Naureen Akhtar; Levini A Msimbira; Mohammed Antar; Shoaib Ashraf; Salik Nawaz Khan; Donald L Smith Journal: Front Microbiol Date: 2022-08-11 Impact factor: 6.064