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Intracolonial genetic variation affects reproductive skew and colony productivity during colony foundation in a parthenogenetic termite

BACKGROUND: In insect societies, intracolonial genetic variation is predicted to affect both colony efficiency and reproductive skew. However, because the effects of genetic variation on these two colony characteristics have been tested independently, it remains unclear whether they are affected by...

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Autores principales: Miyazaki, Satoshi, Yoshimura, Miho, Saiki, Ryota, Hayashi, Yoshinobu, Kitade, Osamu, Tsuji, Kazuki, Maekawa, Kiyoto
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4236541/
https://www.ncbi.nlm.nih.gov/pubmed/25123355
http://dx.doi.org/10.1186/s12862-014-0177-0
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author Miyazaki, Satoshi
Yoshimura, Miho
Saiki, Ryota
Hayashi, Yoshinobu
Kitade, Osamu
Tsuji, Kazuki
Maekawa, Kiyoto
author_facet Miyazaki, Satoshi
Yoshimura, Miho
Saiki, Ryota
Hayashi, Yoshinobu
Kitade, Osamu
Tsuji, Kazuki
Maekawa, Kiyoto
author_sort Miyazaki, Satoshi
collection PubMed
description BACKGROUND: In insect societies, intracolonial genetic variation is predicted to affect both colony efficiency and reproductive skew. However, because the effects of genetic variation on these two colony characteristics have been tested independently, it remains unclear whether they are affected by genetic variation independently or in a related manner. Here we test the effect of genetic variation on colony efficiency and reproductive skew in a rhinotermitid termite, Reticulitermes speratus, a species in which female-female pairs can facultatively found colonies. We established colonies using two types of female-female pairs: colonies founded by sisters (i.e., sister-pair colonies) and those founded by females from different colonies (i.e., unrelated-pair colonies). Colony growth and reproductive skew were then compared between the two types of incipient colonies. RESULTS: At 15 months after colony foundation, unrelated-pair colonies were larger than sister-pair colonies, although the caste ratio between workers and nymphs, which were alternatively differentiated from young larvae, did not differ significantly. Microsatellite DNA analyses of both founders and their parthenogenetically produced offspring indicated that, in both sister-pair and unrelated-pair colonies, there was no significant skew in the production of eggs, larvae, workers and soldiers. Nymph production, however, was significantly more skewed in the sister-pair colonies than in unrelated-pair colonies. Because nymphs can develop into winged adults (alates) or nymphoid reproductives, they have a higher chance of direct reproduction than workers in this species. CONCLUSIONS: Our results support the idea that higher genetic variation among colony members could provide an increase in colony productivity, as shown in hymenopteran social insects. Moreover, this study suggests that low genetic variation (high relatedness) between founding females increases reproductive skew via one female preferentially channeling her relatives along the reproductive track. This study thus demonstrated that, in social insects, intracolonial genetic variation can simultaneously affect both colony efficiency and reproductive skew.
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spelling pubmed-42365412014-11-19 Intracolonial genetic variation affects reproductive skew and colony productivity during colony foundation in a parthenogenetic termite Miyazaki, Satoshi Yoshimura, Miho Saiki, Ryota Hayashi, Yoshinobu Kitade, Osamu Tsuji, Kazuki Maekawa, Kiyoto BMC Evol Biol Research Article BACKGROUND: In insect societies, intracolonial genetic variation is predicted to affect both colony efficiency and reproductive skew. However, because the effects of genetic variation on these two colony characteristics have been tested independently, it remains unclear whether they are affected by genetic variation independently or in a related manner. Here we test the effect of genetic variation on colony efficiency and reproductive skew in a rhinotermitid termite, Reticulitermes speratus, a species in which female-female pairs can facultatively found colonies. We established colonies using two types of female-female pairs: colonies founded by sisters (i.e., sister-pair colonies) and those founded by females from different colonies (i.e., unrelated-pair colonies). Colony growth and reproductive skew were then compared between the two types of incipient colonies. RESULTS: At 15 months after colony foundation, unrelated-pair colonies were larger than sister-pair colonies, although the caste ratio between workers and nymphs, which were alternatively differentiated from young larvae, did not differ significantly. Microsatellite DNA analyses of both founders and their parthenogenetically produced offspring indicated that, in both sister-pair and unrelated-pair colonies, there was no significant skew in the production of eggs, larvae, workers and soldiers. Nymph production, however, was significantly more skewed in the sister-pair colonies than in unrelated-pair colonies. Because nymphs can develop into winged adults (alates) or nymphoid reproductives, they have a higher chance of direct reproduction than workers in this species. CONCLUSIONS: Our results support the idea that higher genetic variation among colony members could provide an increase in colony productivity, as shown in hymenopteran social insects. Moreover, this study suggests that low genetic variation (high relatedness) between founding females increases reproductive skew via one female preferentially channeling her relatives along the reproductive track. This study thus demonstrated that, in social insects, intracolonial genetic variation can simultaneously affect both colony efficiency and reproductive skew. BioMed Central 2014-08-14 /pmc/articles/PMC4236541/ /pubmed/25123355 http://dx.doi.org/10.1186/s12862-014-0177-0 Text en Copyright © 2014 Miyazaki et al.; licensee BioMed Central Ltd http://creativecommons.org/licenses/by/4.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Miyazaki, Satoshi
Yoshimura, Miho
Saiki, Ryota
Hayashi, Yoshinobu
Kitade, Osamu
Tsuji, Kazuki
Maekawa, Kiyoto
Intracolonial genetic variation affects reproductive skew and colony productivity during colony foundation in a parthenogenetic termite
title Intracolonial genetic variation affects reproductive skew and colony productivity during colony foundation in a parthenogenetic termite
title_full Intracolonial genetic variation affects reproductive skew and colony productivity during colony foundation in a parthenogenetic termite
title_fullStr Intracolonial genetic variation affects reproductive skew and colony productivity during colony foundation in a parthenogenetic termite
title_full_unstemmed Intracolonial genetic variation affects reproductive skew and colony productivity during colony foundation in a parthenogenetic termite
title_short Intracolonial genetic variation affects reproductive skew and colony productivity during colony foundation in a parthenogenetic termite
title_sort intracolonial genetic variation affects reproductive skew and colony productivity during colony foundation in a parthenogenetic termite
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4236541/
https://www.ncbi.nlm.nih.gov/pubmed/25123355
http://dx.doi.org/10.1186/s12862-014-0177-0
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