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Repeated loss of variation in insect ovary morphology highlights the role of development in life-history evolution

The number of offspring an organism can produce is a key component of its evolutionary fitness and life history. Here we perform a test of the hypothesized trade-off between the number and size of offspring using thousands of descriptions of the number of egg-producing compartments in the insect ova...

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Autores principales: Church, Samuel H., de Medeiros, Bruno A. S., Donoughe, Seth, Márquez Reyes, Nicole L., Extavour, Cassandra G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8097220/
https://www.ncbi.nlm.nih.gov/pubmed/33947234
http://dx.doi.org/10.1098/rspb.2021.0150
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author Church, Samuel H.
de Medeiros, Bruno A. S.
Donoughe, Seth
Márquez Reyes, Nicole L.
Extavour, Cassandra G.
author_facet Church, Samuel H.
de Medeiros, Bruno A. S.
Donoughe, Seth
Márquez Reyes, Nicole L.
Extavour, Cassandra G.
author_sort Church, Samuel H.
collection PubMed
description The number of offspring an organism can produce is a key component of its evolutionary fitness and life history. Here we perform a test of the hypothesized trade-off between the number and size of offspring using thousands of descriptions of the number of egg-producing compartments in the insect ovary (ovarioles), a common proxy for potential offspring number in insects. We find evidence of a negative relationship between egg size and ovariole number when accounting for adult body size. However, in contrast to prior claims, we note that this relationship is not generalizable across all insect clades, and we highlight several factors that may have contributed to this size-number trade-off being stated as a general rule in previous studies. We reconstruct the evolution of the arrangement of cells that contribute nutrients and patterning information during oogenesis (nurse cells), and show that the diversification of ovariole number and egg size have both been largely independent of their presence or position within the ovariole. Instead, we show that ovariole number evolution has been shaped by a series of transitions between variable and invariant states, with multiple independent lineages evolving to have almost no variation in ovariole number. We highlight the implications of these invariant lineages on our understanding of the specification of ovariole number during development, as well as the importance of considering developmental processes in theories of life-history evolution.
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spelling pubmed-80972202021-05-24 Repeated loss of variation in insect ovary morphology highlights the role of development in life-history evolution Church, Samuel H. de Medeiros, Bruno A. S. Donoughe, Seth Márquez Reyes, Nicole L. Extavour, Cassandra G. Proc Biol Sci Evolution The number of offspring an organism can produce is a key component of its evolutionary fitness and life history. Here we perform a test of the hypothesized trade-off between the number and size of offspring using thousands of descriptions of the number of egg-producing compartments in the insect ovary (ovarioles), a common proxy for potential offspring number in insects. We find evidence of a negative relationship between egg size and ovariole number when accounting for adult body size. However, in contrast to prior claims, we note that this relationship is not generalizable across all insect clades, and we highlight several factors that may have contributed to this size-number trade-off being stated as a general rule in previous studies. We reconstruct the evolution of the arrangement of cells that contribute nutrients and patterning information during oogenesis (nurse cells), and show that the diversification of ovariole number and egg size have both been largely independent of their presence or position within the ovariole. Instead, we show that ovariole number evolution has been shaped by a series of transitions between variable and invariant states, with multiple independent lineages evolving to have almost no variation in ovariole number. We highlight the implications of these invariant lineages on our understanding of the specification of ovariole number during development, as well as the importance of considering developmental processes in theories of life-history evolution. The Royal Society 2021-05-12 2021-05-05 /pmc/articles/PMC8097220/ /pubmed/33947234 http://dx.doi.org/10.1098/rspb.2021.0150 Text en © 2021 The Authors. https://creativecommons.org/licenses/by/4.0/Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, provided the original author and source are credited.
spellingShingle Evolution
Church, Samuel H.
de Medeiros, Bruno A. S.
Donoughe, Seth
Márquez Reyes, Nicole L.
Extavour, Cassandra G.
Repeated loss of variation in insect ovary morphology highlights the role of development in life-history evolution
title Repeated loss of variation in insect ovary morphology highlights the role of development in life-history evolution
title_full Repeated loss of variation in insect ovary morphology highlights the role of development in life-history evolution
title_fullStr Repeated loss of variation in insect ovary morphology highlights the role of development in life-history evolution
title_full_unstemmed Repeated loss of variation in insect ovary morphology highlights the role of development in life-history evolution
title_short Repeated loss of variation in insect ovary morphology highlights the role of development in life-history evolution
title_sort repeated loss of variation in insect ovary morphology highlights the role of development in life-history evolution
topic Evolution
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8097220/
https://www.ncbi.nlm.nih.gov/pubmed/33947234
http://dx.doi.org/10.1098/rspb.2021.0150
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