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Egg Production Constrains Chemical Defenses in a Neotropical Arachnid.

Nazareth TM, Machado G - PLoS ONE (2015)

Bottom Line: In conclusion, females allocate resources to chemical defenses in a way that preserves a primary biological function related to reproduction.However, the trade-off between egg and secretion production makes OFs vulnerable to predators.We suggest that egg production is a critical moment in the life of harvestman females, representing perhaps the highest cost of reproduction in the group.

View Article: PubMed Central - PubMed

Affiliation: Programa de Pós-graduação em Ecologia, Departamento de Ecologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, trav. 14, no. 321, São Paulo, SP, 05508-900, Brazil.

ABSTRACT
Female investment in large eggs increases the demand for fatty acids, which are allocated for yolk production. Since the biosynthetic pathway leading to fatty acids uses the same precursors used in the formation of polyketides, allocation trade-offs are expected to emerge. Therefore, egg production should constrain the investment in chemical defenses based on polyketides, such as benzoquinones. We tested this hypothesis using the harvestman Acutiosoma longipes, which produces large eggs and releases benzoquinones as chemical defense. We predicted that the amount of secretion released by ovigerous females (OFs) would be smaller than that of non-ovigerous females (NOF). We also conducted a series of bioassays in the field and in the laboratory to test whether egg production renders OFs more vulnerable to predation. OFs produce less secretion than NOFs, which is congruent with the hypothesis that egg production constrains the investment in chemical defenses. Results of the bioassays show that the secretion released by OFs is less effective in deterring potential predators (ants and spiders) than the secretion released by NOFs. In conclusion, females allocate resources to chemical defenses in a way that preserves a primary biological function related to reproduction. However, the trade-off between egg and secretion production makes OFs vulnerable to predators. We suggest that egg production is a critical moment in the life of harvestman females, representing perhaps the highest cost of reproduction in the group.

No MeSH data available.


Schematic representation of the of Y model of resource allocation, which proposes that limited resources allocated to reproduction are not available for the rest of the body.In our study, resource input is shown at the left box. Acetate, which is an import precursor of many organic molecules, is acquired when harvestman females feed on live and dead arthropods, fungi, and fruits. The output is shown in the right box illustrating the trade-off between egg production and chemical defenses. The investment in large and heavily yolked eggs in harvestmen (indicated by the white dotted line in the upper photo) increases the demand for fatty acids, which are allocated for the production of the vitelline membrane and lipid droplets imbedded in the yolk. The biosynthetic pathway leading to long chain fatty acids is analogous to the formation of polyketides, and the same precursor (acetate) may be used by both fatty acid synthases (FAS) and polyketide synthases (PKS). Benzoquinones are repellent polyketides produced by many harvestman species in a pair of exocrine glands located at the anterior margins of the carapace (indicated by the white dotted line in the lower photo). As a consequence of allocation trade-offs, the investment in chemical defenses based on benzoquinones should be constrained by egg production.
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pone.0134908.g001: Schematic representation of the of Y model of resource allocation, which proposes that limited resources allocated to reproduction are not available for the rest of the body.In our study, resource input is shown at the left box. Acetate, which is an import precursor of many organic molecules, is acquired when harvestman females feed on live and dead arthropods, fungi, and fruits. The output is shown in the right box illustrating the trade-off between egg production and chemical defenses. The investment in large and heavily yolked eggs in harvestmen (indicated by the white dotted line in the upper photo) increases the demand for fatty acids, which are allocated for the production of the vitelline membrane and lipid droplets imbedded in the yolk. The biosynthetic pathway leading to long chain fatty acids is analogous to the formation of polyketides, and the same precursor (acetate) may be used by both fatty acid synthases (FAS) and polyketide synthases (PKS). Benzoquinones are repellent polyketides produced by many harvestman species in a pair of exocrine glands located at the anterior margins of the carapace (indicated by the white dotted line in the lower photo). As a consequence of allocation trade-offs, the investment in chemical defenses based on benzoquinones should be constrained by egg production.

Mentions: Quinones are polyketides found in the defensive glands of a wide range of arthropod species, including earwigs, cockroaches, termites, grasshoppers, beetles, millipedes, and harvestmen [23]. Despite the great diversity of quinonoid compounds produced by these arthropods, there are only two metabolic pathways for the generation of benzoquinones [27]. In millipedes (Diplopoda) and insects, benzoquinones may be biosynthesized from preformed aromatic rings of amino acids, such as tyrosine, or using acetate or propionate as precursors, suggesting a polyketide origin [27–29, 24]. In harvestmen (Opiliones), however, alkylated benzoquinones seem to be biosynthesized exclusively using acetate and propionate as precursors [27, 30] (Fig 1). According to the Y model of resource allocation, limited resources allocated to reproduction are not available for the soma [6]. Under the perspective of an arthropod female, the investment in large and heavily yolked eggs increases the demand for fatty acids, which are allocated for the production of the vitelline membrane and lipid droplets imbedded in the yolk [31] (Fig 1). Given that the biosynthetic pathways leading to long chain fatty acids are analogous to the formation of polyketides, and that the same precursors are used by both fatty acid synthases and polyketide synthases, allocation trade-offs are expected to emerge [29] (Fig 1).


Egg Production Constrains Chemical Defenses in a Neotropical Arachnid.

Nazareth TM, Machado G - PLoS ONE (2015)

Schematic representation of the of Y model of resource allocation, which proposes that limited resources allocated to reproduction are not available for the rest of the body.In our study, resource input is shown at the left box. Acetate, which is an import precursor of many organic molecules, is acquired when harvestman females feed on live and dead arthropods, fungi, and fruits. The output is shown in the right box illustrating the trade-off between egg production and chemical defenses. The investment in large and heavily yolked eggs in harvestmen (indicated by the white dotted line in the upper photo) increases the demand for fatty acids, which are allocated for the production of the vitelline membrane and lipid droplets imbedded in the yolk. The biosynthetic pathway leading to long chain fatty acids is analogous to the formation of polyketides, and the same precursor (acetate) may be used by both fatty acid synthases (FAS) and polyketide synthases (PKS). Benzoquinones are repellent polyketides produced by many harvestman species in a pair of exocrine glands located at the anterior margins of the carapace (indicated by the white dotted line in the lower photo). As a consequence of allocation trade-offs, the investment in chemical defenses based on benzoquinones should be constrained by egg production.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4557954&req=5

pone.0134908.g001: Schematic representation of the of Y model of resource allocation, which proposes that limited resources allocated to reproduction are not available for the rest of the body.In our study, resource input is shown at the left box. Acetate, which is an import precursor of many organic molecules, is acquired when harvestman females feed on live and dead arthropods, fungi, and fruits. The output is shown in the right box illustrating the trade-off between egg production and chemical defenses. The investment in large and heavily yolked eggs in harvestmen (indicated by the white dotted line in the upper photo) increases the demand for fatty acids, which are allocated for the production of the vitelline membrane and lipid droplets imbedded in the yolk. The biosynthetic pathway leading to long chain fatty acids is analogous to the formation of polyketides, and the same precursor (acetate) may be used by both fatty acid synthases (FAS) and polyketide synthases (PKS). Benzoquinones are repellent polyketides produced by many harvestman species in a pair of exocrine glands located at the anterior margins of the carapace (indicated by the white dotted line in the lower photo). As a consequence of allocation trade-offs, the investment in chemical defenses based on benzoquinones should be constrained by egg production.
Mentions: Quinones are polyketides found in the defensive glands of a wide range of arthropod species, including earwigs, cockroaches, termites, grasshoppers, beetles, millipedes, and harvestmen [23]. Despite the great diversity of quinonoid compounds produced by these arthropods, there are only two metabolic pathways for the generation of benzoquinones [27]. In millipedes (Diplopoda) and insects, benzoquinones may be biosynthesized from preformed aromatic rings of amino acids, such as tyrosine, or using acetate or propionate as precursors, suggesting a polyketide origin [27–29, 24]. In harvestmen (Opiliones), however, alkylated benzoquinones seem to be biosynthesized exclusively using acetate and propionate as precursors [27, 30] (Fig 1). According to the Y model of resource allocation, limited resources allocated to reproduction are not available for the soma [6]. Under the perspective of an arthropod female, the investment in large and heavily yolked eggs increases the demand for fatty acids, which are allocated for the production of the vitelline membrane and lipid droplets imbedded in the yolk [31] (Fig 1). Given that the biosynthetic pathways leading to long chain fatty acids are analogous to the formation of polyketides, and that the same precursors are used by both fatty acid synthases and polyketide synthases, allocation trade-offs are expected to emerge [29] (Fig 1).

Bottom Line: In conclusion, females allocate resources to chemical defenses in a way that preserves a primary biological function related to reproduction.However, the trade-off between egg and secretion production makes OFs vulnerable to predators.We suggest that egg production is a critical moment in the life of harvestman females, representing perhaps the highest cost of reproduction in the group.

View Article: PubMed Central - PubMed

Affiliation: Programa de Pós-graduação em Ecologia, Departamento de Ecologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, trav. 14, no. 321, São Paulo, SP, 05508-900, Brazil.

ABSTRACT
Female investment in large eggs increases the demand for fatty acids, which are allocated for yolk production. Since the biosynthetic pathway leading to fatty acids uses the same precursors used in the formation of polyketides, allocation trade-offs are expected to emerge. Therefore, egg production should constrain the investment in chemical defenses based on polyketides, such as benzoquinones. We tested this hypothesis using the harvestman Acutiosoma longipes, which produces large eggs and releases benzoquinones as chemical defense. We predicted that the amount of secretion released by ovigerous females (OFs) would be smaller than that of non-ovigerous females (NOF). We also conducted a series of bioassays in the field and in the laboratory to test whether egg production renders OFs more vulnerable to predation. OFs produce less secretion than NOFs, which is congruent with the hypothesis that egg production constrains the investment in chemical defenses. Results of the bioassays show that the secretion released by OFs is less effective in deterring potential predators (ants and spiders) than the secretion released by NOFs. In conclusion, females allocate resources to chemical defenses in a way that preserves a primary biological function related to reproduction. However, the trade-off between egg and secretion production makes OFs vulnerable to predators. We suggest that egg production is a critical moment in the life of harvestman females, representing perhaps the highest cost of reproduction in the group.

No MeSH data available.