Cargando…

Variation in rates of spontaneous male production within the nematode species Pristionchus pacificus supports an adaptive role for males and outcrossing

BACKGROUND: The nematode species Pristionchus pacificus has an androdioecious mating system in which populations consist of self-fertilizing hermaphrodites and relatively few males. The prevalence of males in such a system is likely to depend on the relative pros and cons of outcrossing. While outcr...

Descripción completa

Detalles Bibliográficos
Autores principales: Morgan, Katy, McGaughran, Angela, Rödelsperger, Christian, Sommer, Ralf J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5322664/
https://www.ncbi.nlm.nih.gov/pubmed/28228092
http://dx.doi.org/10.1186/s12862-017-0873-7
_version_ 1782509892915953664
author Morgan, Katy
McGaughran, Angela
Rödelsperger, Christian
Sommer, Ralf J.
author_facet Morgan, Katy
McGaughran, Angela
Rödelsperger, Christian
Sommer, Ralf J.
author_sort Morgan, Katy
collection PubMed
description BACKGROUND: The nematode species Pristionchus pacificus has an androdioecious mating system in which populations consist of self-fertilizing hermaphrodites and relatively few males. The prevalence of males in such a system is likely to depend on the relative pros and cons of outcrossing. While outcrossing generates novel allelic combinations and can therefore increase adaptive potential, it may also disrupt the potentially beneficial consequences of repeated generations of selfing. These include purging of deleterious alleles, inheritance of co-adapted allele complexes, improved hermaphrodite fitness and increased population growth. Here we use experimental and population genetic approaches to test hypotheses relating to male production and outcrossing in laboratory and natural populations of P. pacificus sampled from the volcanic island of La Réunion. RESULTS: We find a significant interaction between sampling locality and temperature treatment influencing rates of spontaneous male production in the laboratory. While strains isolated at higher altitude, cooler localities produce a higher proportion of male offspring at 25 °C relative to 20 or 15 °C, the reverse pattern is seen in strains isolated from warmer, low altitude localities. Linkage disequilibrium extends across long physical distances, but fails to approach levels reported for the partially selfing nematode species Caenorhabditis elegans. Finally, we find evidence for admixture between divergent genetic lineages. CONCLUSIONS: Elevated rates of laboratory male generation appear to occur under environmental conditions which differ from those experienced by populations in nature. Such elevated male generation may result in higher outcrossing rates, hence driving increased effective recombination and the creation of potentially adaptive novel allelic combinations. Patterns of linkage disequilibrium decay support selfing as the predominant reproductive strategy in P. pacificus. Finally, despite the potential for outcrossing depression, our results suggest admixture has occurred between distinct genetic lineages since their independent colonization of the island, suggesting outcrossing depression may not be uniform in this species. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-017-0873-7) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-5322664
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-53226642017-03-01 Variation in rates of spontaneous male production within the nematode species Pristionchus pacificus supports an adaptive role for males and outcrossing Morgan, Katy McGaughran, Angela Rödelsperger, Christian Sommer, Ralf J. BMC Evol Biol Research Article BACKGROUND: The nematode species Pristionchus pacificus has an androdioecious mating system in which populations consist of self-fertilizing hermaphrodites and relatively few males. The prevalence of males in such a system is likely to depend on the relative pros and cons of outcrossing. While outcrossing generates novel allelic combinations and can therefore increase adaptive potential, it may also disrupt the potentially beneficial consequences of repeated generations of selfing. These include purging of deleterious alleles, inheritance of co-adapted allele complexes, improved hermaphrodite fitness and increased population growth. Here we use experimental and population genetic approaches to test hypotheses relating to male production and outcrossing in laboratory and natural populations of P. pacificus sampled from the volcanic island of La Réunion. RESULTS: We find a significant interaction between sampling locality and temperature treatment influencing rates of spontaneous male production in the laboratory. While strains isolated at higher altitude, cooler localities produce a higher proportion of male offspring at 25 °C relative to 20 or 15 °C, the reverse pattern is seen in strains isolated from warmer, low altitude localities. Linkage disequilibrium extends across long physical distances, but fails to approach levels reported for the partially selfing nematode species Caenorhabditis elegans. Finally, we find evidence for admixture between divergent genetic lineages. CONCLUSIONS: Elevated rates of laboratory male generation appear to occur under environmental conditions which differ from those experienced by populations in nature. Such elevated male generation may result in higher outcrossing rates, hence driving increased effective recombination and the creation of potentially adaptive novel allelic combinations. Patterns of linkage disequilibrium decay support selfing as the predominant reproductive strategy in P. pacificus. Finally, despite the potential for outcrossing depression, our results suggest admixture has occurred between distinct genetic lineages since their independent colonization of the island, suggesting outcrossing depression may not be uniform in this species. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-017-0873-7) contains supplementary material, which is available to authorized users. BioMed Central 2017-02-23 /pmc/articles/PMC5322664/ /pubmed/28228092 http://dx.doi.org/10.1186/s12862-017-0873-7 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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
Morgan, Katy
McGaughran, Angela
Rödelsperger, Christian
Sommer, Ralf J.
Variation in rates of spontaneous male production within the nematode species Pristionchus pacificus supports an adaptive role for males and outcrossing
title Variation in rates of spontaneous male production within the nematode species Pristionchus pacificus supports an adaptive role for males and outcrossing
title_full Variation in rates of spontaneous male production within the nematode species Pristionchus pacificus supports an adaptive role for males and outcrossing
title_fullStr Variation in rates of spontaneous male production within the nematode species Pristionchus pacificus supports an adaptive role for males and outcrossing
title_full_unstemmed Variation in rates of spontaneous male production within the nematode species Pristionchus pacificus supports an adaptive role for males and outcrossing
title_short Variation in rates of spontaneous male production within the nematode species Pristionchus pacificus supports an adaptive role for males and outcrossing
title_sort variation in rates of spontaneous male production within the nematode species pristionchus pacificus supports an adaptive role for males and outcrossing
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5322664/
https://www.ncbi.nlm.nih.gov/pubmed/28228092
http://dx.doi.org/10.1186/s12862-017-0873-7
work_keys_str_mv AT morgankaty variationinratesofspontaneousmaleproductionwithinthenematodespeciespristionchuspacificussupportsanadaptiveroleformalesandoutcrossing
AT mcgaughranangela variationinratesofspontaneousmaleproductionwithinthenematodespeciespristionchuspacificussupportsanadaptiveroleformalesandoutcrossing
AT rodelspergerchristian variationinratesofspontaneousmaleproductionwithinthenematodespeciespristionchuspacificussupportsanadaptiveroleformalesandoutcrossing
AT sommerralfj variationinratesofspontaneousmaleproductionwithinthenematodespeciespristionchuspacificussupportsanadaptiveroleformalesandoutcrossing