Colony level fitness analysis identifies a trade-off between population growth rate and dauer yield in Caenorhabditis elegans
Background In the evolution from unicellular to multicellular life forms, natural selection favored reduced cell proliferation and even programmed cell death if this increased organismal fitness. Could reduced individual fertility or even programmed organismal death similarly increase the fitness of...
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| Autor*in: |
Chapman, Hannah [verfasserIn] |
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| Format: |
E-Artikel |
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| Sprache: |
Englisch |
| Erschienen: |
2024 |
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© The Author(s) 2024 |
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Enthalten in: BMC evolutionary biology - London : BioMed Central, 2001, 24(2024), 1 vom: 25. Jan. |
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| Übergeordnetes Werk: |
volume:24 ; year:2024 ; number:1 ; day:25 ; month:01 |
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| DOI / URN: |
10.1186/s12862-024-02199-1 |
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SPR054509246 |
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| 520 | |a Background In the evolution from unicellular to multicellular life forms, natural selection favored reduced cell proliferation and even programmed cell death if this increased organismal fitness. Could reduced individual fertility or even programmed organismal death similarly increase the fitness of colonies of closely-related metazoan organisms? This possibility is at least consistent with evolutionary theory, and has been supported by computer modelling. Caenorhabditis elegans has a boom and bust life history, where populations of nematodes that are sometimes near clonal subsist on and consume food patches, and then generate dauer larva dispersal propagules. A recent study of an in silico model of C. elegans predicted that one determinant of colony fitness (measured as dauer yield) is minimization of futile food consumption (i.e. that which does not contribute to dauer yield). One way to achieve this is to optimize colony population structure by adjustment of individual fertility. Results Here we describe development of a C. elegans colony fitness assay, and its use to investigate the effect of altering population structure on colony fitness after population bust. Fitness metrics measured were speed of dauer production, and dauer yield, an indirect measure of efficiency of resource utilization (i.e. conversion of food into dauers). We find that with increasing founder number, speed of dauer production increases (due to earlier bust) but dauer yield rises and falls. In addition, some dauer recovery was detected soon after the post-colony bust peak of dauer yield, suggesting possible bet hedging among dauers. Conclusions These results suggest the presence of a fitness trade-off at colony level between speed and efficiency of resource utilization in C. elegans. They also provide indirect evidence that population structure is a determinant of colony level fitness, potentially by affecting level of futile food consumption. | ||
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10.1186/s12862-024-02199-1 doi (DE-627)SPR054509246 (SPR)s12862-024-02199-1-e DE-627 ger DE-627 rakwb eng Chapman, Hannah verfasserin aut Colony level fitness analysis identifies a trade-off between population growth rate and dauer yield in Caenorhabditis elegans 2024 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier © The Author(s) 2024 Background In the evolution from unicellular to multicellular life forms, natural selection favored reduced cell proliferation and even programmed cell death if this increased organismal fitness. Could reduced individual fertility or even programmed organismal death similarly increase the fitness of colonies of closely-related metazoan organisms? This possibility is at least consistent with evolutionary theory, and has been supported by computer modelling. Caenorhabditis elegans has a boom and bust life history, where populations of nematodes that are sometimes near clonal subsist on and consume food patches, and then generate dauer larva dispersal propagules. A recent study of an in silico model of C. elegans predicted that one determinant of colony fitness (measured as dauer yield) is minimization of futile food consumption (i.e. that which does not contribute to dauer yield). One way to achieve this is to optimize colony population structure by adjustment of individual fertility. Results Here we describe development of a C. elegans colony fitness assay, and its use to investigate the effect of altering population structure on colony fitness after population bust. Fitness metrics measured were speed of dauer production, and dauer yield, an indirect measure of efficiency of resource utilization (i.e. conversion of food into dauers). We find that with increasing founder number, speed of dauer production increases (due to earlier bust) but dauer yield rises and falls. In addition, some dauer recovery was detected soon after the post-colony bust peak of dauer yield, suggesting possible bet hedging among dauers. Conclusions These results suggest the presence of a fitness trade-off at colony level between speed and efficiency of resource utilization in C. elegans. They also provide indirect evidence that population structure is a determinant of colony level fitness, potentially by affecting level of futile food consumption. Adaptive death (dpeaa)DE-He213 ecology (dpeaa)DE-He213 Evolution of aging (dpeaa)DE-He213 Inclusive fitness (dpeaa)DE-He213 Trade-off (dpeaa)DE-He213 Hsiung, Kuei Ching aut Rawlinson, Isadora aut Galimov, Evgeniy R. aut Gems, David aut Enthalten in BMC evolutionary biology London : BioMed Central, 2001 24(2024), 1 vom: 25. Jan. (DE-627)32664489X (DE-600)2041493-6 1471-2148 nnns volume:24 year:2024 number:1 day:25 month:01 https://dx.doi.org/10.1186/s12862-024-02199-1 kostenfrei Volltext GBV_USEFLAG_A SYSFLAG_A GBV_SPRINGER GBV_ILN_2021 AR 24 2024 1 25 01 |
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10.1186/s12862-024-02199-1 doi (DE-627)SPR054509246 (SPR)s12862-024-02199-1-e DE-627 ger DE-627 rakwb eng Chapman, Hannah verfasserin aut Colony level fitness analysis identifies a trade-off between population growth rate and dauer yield in Caenorhabditis elegans 2024 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier © The Author(s) 2024 Background In the evolution from unicellular to multicellular life forms, natural selection favored reduced cell proliferation and even programmed cell death if this increased organismal fitness. Could reduced individual fertility or even programmed organismal death similarly increase the fitness of colonies of closely-related metazoan organisms? This possibility is at least consistent with evolutionary theory, and has been supported by computer modelling. Caenorhabditis elegans has a boom and bust life history, where populations of nematodes that are sometimes near clonal subsist on and consume food patches, and then generate dauer larva dispersal propagules. A recent study of an in silico model of C. elegans predicted that one determinant of colony fitness (measured as dauer yield) is minimization of futile food consumption (i.e. that which does not contribute to dauer yield). One way to achieve this is to optimize colony population structure by adjustment of individual fertility. Results Here we describe development of a C. elegans colony fitness assay, and its use to investigate the effect of altering population structure on colony fitness after population bust. Fitness metrics measured were speed of dauer production, and dauer yield, an indirect measure of efficiency of resource utilization (i.e. conversion of food into dauers). We find that with increasing founder number, speed of dauer production increases (due to earlier bust) but dauer yield rises and falls. In addition, some dauer recovery was detected soon after the post-colony bust peak of dauer yield, suggesting possible bet hedging among dauers. Conclusions These results suggest the presence of a fitness trade-off at colony level between speed and efficiency of resource utilization in C. elegans. They also provide indirect evidence that population structure is a determinant of colony level fitness, potentially by affecting level of futile food consumption. Adaptive death (dpeaa)DE-He213 ecology (dpeaa)DE-He213 Evolution of aging (dpeaa)DE-He213 Inclusive fitness (dpeaa)DE-He213 Trade-off (dpeaa)DE-He213 Hsiung, Kuei Ching aut Rawlinson, Isadora aut Galimov, Evgeniy R. aut Gems, David aut Enthalten in BMC evolutionary biology London : BioMed Central, 2001 24(2024), 1 vom: 25. Jan. (DE-627)32664489X (DE-600)2041493-6 1471-2148 nnns volume:24 year:2024 number:1 day:25 month:01 https://dx.doi.org/10.1186/s12862-024-02199-1 kostenfrei Volltext GBV_USEFLAG_A SYSFLAG_A GBV_SPRINGER GBV_ILN_2021 AR 24 2024 1 25 01 |
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10.1186/s12862-024-02199-1 doi (DE-627)SPR054509246 (SPR)s12862-024-02199-1-e DE-627 ger DE-627 rakwb eng Chapman, Hannah verfasserin aut Colony level fitness analysis identifies a trade-off between population growth rate and dauer yield in Caenorhabditis elegans 2024 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier © The Author(s) 2024 Background In the evolution from unicellular to multicellular life forms, natural selection favored reduced cell proliferation and even programmed cell death if this increased organismal fitness. Could reduced individual fertility or even programmed organismal death similarly increase the fitness of colonies of closely-related metazoan organisms? This possibility is at least consistent with evolutionary theory, and has been supported by computer modelling. Caenorhabditis elegans has a boom and bust life history, where populations of nematodes that are sometimes near clonal subsist on and consume food patches, and then generate dauer larva dispersal propagules. A recent study of an in silico model of C. elegans predicted that one determinant of colony fitness (measured as dauer yield) is minimization of futile food consumption (i.e. that which does not contribute to dauer yield). One way to achieve this is to optimize colony population structure by adjustment of individual fertility. Results Here we describe development of a C. elegans colony fitness assay, and its use to investigate the effect of altering population structure on colony fitness after population bust. Fitness metrics measured were speed of dauer production, and dauer yield, an indirect measure of efficiency of resource utilization (i.e. conversion of food into dauers). We find that with increasing founder number, speed of dauer production increases (due to earlier bust) but dauer yield rises and falls. In addition, some dauer recovery was detected soon after the post-colony bust peak of dauer yield, suggesting possible bet hedging among dauers. Conclusions These results suggest the presence of a fitness trade-off at colony level between speed and efficiency of resource utilization in C. elegans. They also provide indirect evidence that population structure is a determinant of colony level fitness, potentially by affecting level of futile food consumption. Adaptive death (dpeaa)DE-He213 ecology (dpeaa)DE-He213 Evolution of aging (dpeaa)DE-He213 Inclusive fitness (dpeaa)DE-He213 Trade-off (dpeaa)DE-He213 Hsiung, Kuei Ching aut Rawlinson, Isadora aut Galimov, Evgeniy R. aut Gems, David aut Enthalten in BMC evolutionary biology London : BioMed Central, 2001 24(2024), 1 vom: 25. Jan. (DE-627)32664489X (DE-600)2041493-6 1471-2148 nnns volume:24 year:2024 number:1 day:25 month:01 https://dx.doi.org/10.1186/s12862-024-02199-1 kostenfrei Volltext GBV_USEFLAG_A SYSFLAG_A GBV_SPRINGER GBV_ILN_2021 AR 24 2024 1 25 01 |
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10.1186/s12862-024-02199-1 doi (DE-627)SPR054509246 (SPR)s12862-024-02199-1-e DE-627 ger DE-627 rakwb eng Chapman, Hannah verfasserin aut Colony level fitness analysis identifies a trade-off between population growth rate and dauer yield in Caenorhabditis elegans 2024 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier © The Author(s) 2024 Background In the evolution from unicellular to multicellular life forms, natural selection favored reduced cell proliferation and even programmed cell death if this increased organismal fitness. Could reduced individual fertility or even programmed organismal death similarly increase the fitness of colonies of closely-related metazoan organisms? This possibility is at least consistent with evolutionary theory, and has been supported by computer modelling. Caenorhabditis elegans has a boom and bust life history, where populations of nematodes that are sometimes near clonal subsist on and consume food patches, and then generate dauer larva dispersal propagules. A recent study of an in silico model of C. elegans predicted that one determinant of colony fitness (measured as dauer yield) is minimization of futile food consumption (i.e. that which does not contribute to dauer yield). One way to achieve this is to optimize colony population structure by adjustment of individual fertility. Results Here we describe development of a C. elegans colony fitness assay, and its use to investigate the effect of altering population structure on colony fitness after population bust. Fitness metrics measured were speed of dauer production, and dauer yield, an indirect measure of efficiency of resource utilization (i.e. conversion of food into dauers). We find that with increasing founder number, speed of dauer production increases (due to earlier bust) but dauer yield rises and falls. In addition, some dauer recovery was detected soon after the post-colony bust peak of dauer yield, suggesting possible bet hedging among dauers. Conclusions These results suggest the presence of a fitness trade-off at colony level between speed and efficiency of resource utilization in C. elegans. They also provide indirect evidence that population structure is a determinant of colony level fitness, potentially by affecting level of futile food consumption. Adaptive death (dpeaa)DE-He213 ecology (dpeaa)DE-He213 Evolution of aging (dpeaa)DE-He213 Inclusive fitness (dpeaa)DE-He213 Trade-off (dpeaa)DE-He213 Hsiung, Kuei Ching aut Rawlinson, Isadora aut Galimov, Evgeniy R. aut Gems, David aut Enthalten in BMC evolutionary biology London : BioMed Central, 2001 24(2024), 1 vom: 25. Jan. (DE-627)32664489X (DE-600)2041493-6 1471-2148 nnns volume:24 year:2024 number:1 day:25 month:01 https://dx.doi.org/10.1186/s12862-024-02199-1 kostenfrei Volltext GBV_USEFLAG_A SYSFLAG_A GBV_SPRINGER GBV_ILN_2021 AR 24 2024 1 25 01 |
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10.1186/s12862-024-02199-1 doi (DE-627)SPR054509246 (SPR)s12862-024-02199-1-e DE-627 ger DE-627 rakwb eng Chapman, Hannah verfasserin aut Colony level fitness analysis identifies a trade-off between population growth rate and dauer yield in Caenorhabditis elegans 2024 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier © The Author(s) 2024 Background In the evolution from unicellular to multicellular life forms, natural selection favored reduced cell proliferation and even programmed cell death if this increased organismal fitness. Could reduced individual fertility or even programmed organismal death similarly increase the fitness of colonies of closely-related metazoan organisms? This possibility is at least consistent with evolutionary theory, and has been supported by computer modelling. Caenorhabditis elegans has a boom and bust life history, where populations of nematodes that are sometimes near clonal subsist on and consume food patches, and then generate dauer larva dispersal propagules. A recent study of an in silico model of C. elegans predicted that one determinant of colony fitness (measured as dauer yield) is minimization of futile food consumption (i.e. that which does not contribute to dauer yield). One way to achieve this is to optimize colony population structure by adjustment of individual fertility. Results Here we describe development of a C. elegans colony fitness assay, and its use to investigate the effect of altering population structure on colony fitness after population bust. Fitness metrics measured were speed of dauer production, and dauer yield, an indirect measure of efficiency of resource utilization (i.e. conversion of food into dauers). We find that with increasing founder number, speed of dauer production increases (due to earlier bust) but dauer yield rises and falls. In addition, some dauer recovery was detected soon after the post-colony bust peak of dauer yield, suggesting possible bet hedging among dauers. Conclusions These results suggest the presence of a fitness trade-off at colony level between speed and efficiency of resource utilization in C. elegans. They also provide indirect evidence that population structure is a determinant of colony level fitness, potentially by affecting level of futile food consumption. Adaptive death (dpeaa)DE-He213 ecology (dpeaa)DE-He213 Evolution of aging (dpeaa)DE-He213 Inclusive fitness (dpeaa)DE-He213 Trade-off (dpeaa)DE-He213 Hsiung, Kuei Ching aut Rawlinson, Isadora aut Galimov, Evgeniy R. aut Gems, David aut Enthalten in BMC evolutionary biology London : BioMed Central, 2001 24(2024), 1 vom: 25. Jan. (DE-627)32664489X (DE-600)2041493-6 1471-2148 nnns volume:24 year:2024 number:1 day:25 month:01 https://dx.doi.org/10.1186/s12862-024-02199-1 kostenfrei Volltext GBV_USEFLAG_A SYSFLAG_A GBV_SPRINGER GBV_ILN_2021 AR 24 2024 1 25 01 |
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Colony level fitness analysis identifies a trade-off between population growth rate and dauer yield in Caenorhabditis elegans |
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Colony level fitness analysis identifies a trade-off between population growth rate and dauer yield in Caenorhabditis elegans |
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Chapman, Hannah |
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Chapman, Hannah Hsiung, Kuei Ching Rawlinson, Isadora Galimov, Evgeniy R. Gems, David |
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colony level fitness analysis identifies a trade-off between population growth rate and dauer yield in caenorhabditis elegans |
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Colony level fitness analysis identifies a trade-off between population growth rate and dauer yield in Caenorhabditis elegans |
| abstract |
Background In the evolution from unicellular to multicellular life forms, natural selection favored reduced cell proliferation and even programmed cell death if this increased organismal fitness. Could reduced individual fertility or even programmed organismal death similarly increase the fitness of colonies of closely-related metazoan organisms? This possibility is at least consistent with evolutionary theory, and has been supported by computer modelling. Caenorhabditis elegans has a boom and bust life history, where populations of nematodes that are sometimes near clonal subsist on and consume food patches, and then generate dauer larva dispersal propagules. A recent study of an in silico model of C. elegans predicted that one determinant of colony fitness (measured as dauer yield) is minimization of futile food consumption (i.e. that which does not contribute to dauer yield). One way to achieve this is to optimize colony population structure by adjustment of individual fertility. Results Here we describe development of a C. elegans colony fitness assay, and its use to investigate the effect of altering population structure on colony fitness after population bust. Fitness metrics measured were speed of dauer production, and dauer yield, an indirect measure of efficiency of resource utilization (i.e. conversion of food into dauers). We find that with increasing founder number, speed of dauer production increases (due to earlier bust) but dauer yield rises and falls. In addition, some dauer recovery was detected soon after the post-colony bust peak of dauer yield, suggesting possible bet hedging among dauers. Conclusions These results suggest the presence of a fitness trade-off at colony level between speed and efficiency of resource utilization in C. elegans. They also provide indirect evidence that population structure is a determinant of colony level fitness, potentially by affecting level of futile food consumption. © The Author(s) 2024 |
| abstractGer |
Background In the evolution from unicellular to multicellular life forms, natural selection favored reduced cell proliferation and even programmed cell death if this increased organismal fitness. Could reduced individual fertility or even programmed organismal death similarly increase the fitness of colonies of closely-related metazoan organisms? This possibility is at least consistent with evolutionary theory, and has been supported by computer modelling. Caenorhabditis elegans has a boom and bust life history, where populations of nematodes that are sometimes near clonal subsist on and consume food patches, and then generate dauer larva dispersal propagules. A recent study of an in silico model of C. elegans predicted that one determinant of colony fitness (measured as dauer yield) is minimization of futile food consumption (i.e. that which does not contribute to dauer yield). One way to achieve this is to optimize colony population structure by adjustment of individual fertility. Results Here we describe development of a C. elegans colony fitness assay, and its use to investigate the effect of altering population structure on colony fitness after population bust. Fitness metrics measured were speed of dauer production, and dauer yield, an indirect measure of efficiency of resource utilization (i.e. conversion of food into dauers). We find that with increasing founder number, speed of dauer production increases (due to earlier bust) but dauer yield rises and falls. In addition, some dauer recovery was detected soon after the post-colony bust peak of dauer yield, suggesting possible bet hedging among dauers. Conclusions These results suggest the presence of a fitness trade-off at colony level between speed and efficiency of resource utilization in C. elegans. They also provide indirect evidence that population structure is a determinant of colony level fitness, potentially by affecting level of futile food consumption. © The Author(s) 2024 |
| abstract_unstemmed |
Background In the evolution from unicellular to multicellular life forms, natural selection favored reduced cell proliferation and even programmed cell death if this increased organismal fitness. Could reduced individual fertility or even programmed organismal death similarly increase the fitness of colonies of closely-related metazoan organisms? This possibility is at least consistent with evolutionary theory, and has been supported by computer modelling. Caenorhabditis elegans has a boom and bust life history, where populations of nematodes that are sometimes near clonal subsist on and consume food patches, and then generate dauer larva dispersal propagules. A recent study of an in silico model of C. elegans predicted that one determinant of colony fitness (measured as dauer yield) is minimization of futile food consumption (i.e. that which does not contribute to dauer yield). One way to achieve this is to optimize colony population structure by adjustment of individual fertility. Results Here we describe development of a C. elegans colony fitness assay, and its use to investigate the effect of altering population structure on colony fitness after population bust. Fitness metrics measured were speed of dauer production, and dauer yield, an indirect measure of efficiency of resource utilization (i.e. conversion of food into dauers). We find that with increasing founder number, speed of dauer production increases (due to earlier bust) but dauer yield rises and falls. In addition, some dauer recovery was detected soon after the post-colony bust peak of dauer yield, suggesting possible bet hedging among dauers. Conclusions These results suggest the presence of a fitness trade-off at colony level between speed and efficiency of resource utilization in C. elegans. They also provide indirect evidence that population structure is a determinant of colony level fitness, potentially by affecting level of futile food consumption. © The Author(s) 2024 |
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Colony level fitness analysis identifies a trade-off between population growth rate and dauer yield in Caenorhabditis elegans |
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Hsiung, Kuei Ching Rawlinson, Isadora Galimov, Evgeniy R. Gems, David |
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