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Phenotypic plasticity and modularity allow for the production of novel mosaic phenotypes in ants.

Londe S, Monnin T, Cornette R, Debat V, Fisher BL, Molet M - Evodevo (2015)

Bottom Line: In addition, we found that many other individuals traditionally classified as workers or queens also exhibit some level of mosaicism.Indeed, we found that most mosaics have queen-like head and gaster but a worker-like thorax congruent with the morphology of ergatoid queens and soldiers, respectively.Ergatoid queens of M. oberthueri, a sister species of M. rogeri, could have evolved from intercastes produced ancestrally through such a process.

View Article: PubMed Central - PubMed

Affiliation: UMR 7618 Institute of Ecology and Environmental Sciences of Paris, Sorbonne Universités, UPMC Univ Paris 06, 7 quai St Bernard, 75 252 Paris, France.

ABSTRACT

Background: The origin of discrete novelties remains unclear. Some authors suggest that qualitative phenotypic changes may result from the reorganization of preexisting phenotypic traits during development (i.e., developmental recombination) following genetic or environmental changes. Because ants combine high modularity with extreme phenotypic plasticity (queen and worker castes), their diversified castes could have evolved by developmental recombination. We performed a quantitative morphometric study to investigate the developmental origins of novel phenotypes in the ant Mystrium rogeri, which occasionally produces anomalous 'intercastes.' Our analysis compared the variation of six morphological modules with body size using a large sample of intercastes.

Results: We confirmed that intercastes are conspicuous mosaics that recombine queen and worker modules. In addition, we found that many other individuals traditionally classified as workers or queens also exhibit some level of mosaicism. The six modules had distinct profiles of variation suggesting that each module responds differentially to factors that control body size and polyphenism. Mosaicism appears to result from each module responding differently yet in an ordered and predictable manner to intermediate levels of inducing factors that control polyphenism. The order of module response determines which mosaic combinations are produced.

Conclusions: Because the frequency of mosaics and their canalization around a particular phenotype may evolve by selection on standing genetic variation that affects the plastic response (i.e., genetic accommodation), developmental recombination is likely to play an important role in the evolution of novel castes in ants. Indeed, we found that most mosaics have queen-like head and gaster but a worker-like thorax congruent with the morphology of ergatoid queens and soldiers, respectively. Ergatoid queens of M. oberthueri, a sister species of M. rogeri, could have evolved from intercastes produced ancestrally through such a process.

No MeSH data available.


Hypothesis for the developmental origin of mosaic phenotypes. Each larva may develop into a queen or a worker depending on determining factors experienced during its ontogeny. In ants, determining factors are mainly environmental, although genetic influences have also been found in some species. If different modules respond differently to determining factors, intermediate levels of these factors induce the production of mosaic individuals with queen-like morphology for some modules and worker-like morphology for others. For instance, the intercaste depicted here (vertical line for intermediate value of determining factors) has a queen-like module 1 but a worker-like module 2
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Fig1: Hypothesis for the developmental origin of mosaic phenotypes. Each larva may develop into a queen or a worker depending on determining factors experienced during its ontogeny. In ants, determining factors are mainly environmental, although genetic influences have also been found in some species. If different modules respond differently to determining factors, intermediate levels of these factors induce the production of mosaic individuals with queen-like morphology for some modules and worker-like morphology for others. For instance, the intercaste depicted here (vertical line for intermediate value of determining factors) has a queen-like module 1 but a worker-like module 2

Mentions: In this study, we do not investigate the genetic determinants of the evolutionary changes leading to intercastes. Many mutational mechanisms may cause these changes. Instead, we analyze the final product of developmental processes, i.e., phenotypes. That is, we focus on the level directly visible to natural selection. We propose that mosaic phenotypes may be produced in ants because the latter exhibits a high degree of modularity and phenotypic plasticity. Indeed, if different modules have different response thresholds to the same inducing factor, mosaic phenotypes may be generated by intermediate levels of factors inducing differential responses among modules (Fig. 1). In most cases, normal workers and winged queens would be produced because the levels of inducing factors are far above or far below the response thresholds of all modules. However, on the rare occasions where intermediate levels of inducing factors are experienced, some modules within one larva may develop as in workers, whereas others may develop as in queens, thereby resulting in a mosaic individual combining worker and queen phenotypic traits. This hypothesis has two corollaries that we test in this study: (1) Modules have distinct patterns of variation in response to caste-determining factors. This causes a differential response among modules for intermediate values of caste-determining factors. (2) The range of possible mosaic phenotypes is strongly constrained by the distinct patterns of variation of the different modules. Finally, we discuss the developmental origins of mosaic phenotypes and their significance regarding the model of developmental recombination and the multiple evolutions of ergatoid queens and soldiers in ants.Fig. 1


Phenotypic plasticity and modularity allow for the production of novel mosaic phenotypes in ants.

Londe S, Monnin T, Cornette R, Debat V, Fisher BL, Molet M - Evodevo (2015)

Hypothesis for the developmental origin of mosaic phenotypes. Each larva may develop into a queen or a worker depending on determining factors experienced during its ontogeny. In ants, determining factors are mainly environmental, although genetic influences have also been found in some species. If different modules respond differently to determining factors, intermediate levels of these factors induce the production of mosaic individuals with queen-like morphology for some modules and worker-like morphology for others. For instance, the intercaste depicted here (vertical line for intermediate value of determining factors) has a queen-like module 1 but a worker-like module 2
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4666092&req=5

Fig1: Hypothesis for the developmental origin of mosaic phenotypes. Each larva may develop into a queen or a worker depending on determining factors experienced during its ontogeny. In ants, determining factors are mainly environmental, although genetic influences have also been found in some species. If different modules respond differently to determining factors, intermediate levels of these factors induce the production of mosaic individuals with queen-like morphology for some modules and worker-like morphology for others. For instance, the intercaste depicted here (vertical line for intermediate value of determining factors) has a queen-like module 1 but a worker-like module 2
Mentions: In this study, we do not investigate the genetic determinants of the evolutionary changes leading to intercastes. Many mutational mechanisms may cause these changes. Instead, we analyze the final product of developmental processes, i.e., phenotypes. That is, we focus on the level directly visible to natural selection. We propose that mosaic phenotypes may be produced in ants because the latter exhibits a high degree of modularity and phenotypic plasticity. Indeed, if different modules have different response thresholds to the same inducing factor, mosaic phenotypes may be generated by intermediate levels of factors inducing differential responses among modules (Fig. 1). In most cases, normal workers and winged queens would be produced because the levels of inducing factors are far above or far below the response thresholds of all modules. However, on the rare occasions where intermediate levels of inducing factors are experienced, some modules within one larva may develop as in workers, whereas others may develop as in queens, thereby resulting in a mosaic individual combining worker and queen phenotypic traits. This hypothesis has two corollaries that we test in this study: (1) Modules have distinct patterns of variation in response to caste-determining factors. This causes a differential response among modules for intermediate values of caste-determining factors. (2) The range of possible mosaic phenotypes is strongly constrained by the distinct patterns of variation of the different modules. Finally, we discuss the developmental origins of mosaic phenotypes and their significance regarding the model of developmental recombination and the multiple evolutions of ergatoid queens and soldiers in ants.Fig. 1

Bottom Line: In addition, we found that many other individuals traditionally classified as workers or queens also exhibit some level of mosaicism.Indeed, we found that most mosaics have queen-like head and gaster but a worker-like thorax congruent with the morphology of ergatoid queens and soldiers, respectively.Ergatoid queens of M. oberthueri, a sister species of M. rogeri, could have evolved from intercastes produced ancestrally through such a process.

View Article: PubMed Central - PubMed

Affiliation: UMR 7618 Institute of Ecology and Environmental Sciences of Paris, Sorbonne Universités, UPMC Univ Paris 06, 7 quai St Bernard, 75 252 Paris, France.

ABSTRACT

Background: The origin of discrete novelties remains unclear. Some authors suggest that qualitative phenotypic changes may result from the reorganization of preexisting phenotypic traits during development (i.e., developmental recombination) following genetic or environmental changes. Because ants combine high modularity with extreme phenotypic plasticity (queen and worker castes), their diversified castes could have evolved by developmental recombination. We performed a quantitative morphometric study to investigate the developmental origins of novel phenotypes in the ant Mystrium rogeri, which occasionally produces anomalous 'intercastes.' Our analysis compared the variation of six morphological modules with body size using a large sample of intercastes.

Results: We confirmed that intercastes are conspicuous mosaics that recombine queen and worker modules. In addition, we found that many other individuals traditionally classified as workers or queens also exhibit some level of mosaicism. The six modules had distinct profiles of variation suggesting that each module responds differentially to factors that control body size and polyphenism. Mosaicism appears to result from each module responding differently yet in an ordered and predictable manner to intermediate levels of inducing factors that control polyphenism. The order of module response determines which mosaic combinations are produced.

Conclusions: Because the frequency of mosaics and their canalization around a particular phenotype may evolve by selection on standing genetic variation that affects the plastic response (i.e., genetic accommodation), developmental recombination is likely to play an important role in the evolution of novel castes in ants. Indeed, we found that most mosaics have queen-like head and gaster but a worker-like thorax congruent with the morphology of ergatoid queens and soldiers, respectively. Ergatoid queens of M. oberthueri, a sister species of M. rogeri, could have evolved from intercastes produced ancestrally through such a process.

No MeSH data available.