Limits...
Dispersal strategies of phytophagous insects at a local scale: adaptive potential of aphids in an agricultural environment.

Lombaert E, Boll R, Lapchin L - BMC Evol. Biol. (2006)

Bottom Line: The spread of agriculture greatly modified the selective pressures exerted by plants on phytophagous insects, by providing these insects with a high-level resource, structured in time and space.The life history, behavioural and physiological traits of some insect species may have evolved in response to these changes, allowing them to crowd on crops and to become agricultural pests.Dispersal, which is one of these traits, is a key concept in evolutionary biology but has been over-simplified in most theoretical studies.

View Article: PubMed Central - HTML - PubMed

Affiliation: Unité de Lutte Biologique, INRA, 06903 Sophia-Antipolis, France. lombaert@antibes.inra.fr

ABSTRACT

Background: The spread of agriculture greatly modified the selective pressures exerted by plants on phytophagous insects, by providing these insects with a high-level resource, structured in time and space. The life history, behavioural and physiological traits of some insect species may have evolved in response to these changes, allowing them to crowd on crops and to become agricultural pests. Dispersal, which is one of these traits, is a key concept in evolutionary biology but has been over-simplified in most theoretical studies. We evaluated the impact of the local-scale dispersal strategy of phytophagous insects on their fitness, using an individual-based model to simulate population dynamics and dispersal between leaves and plants, by walking and flying, of the aphid Aphis gossypii, a major agricultural pest, in a melon field. We compared the optimal values for dispersal parameters in the model with the corresponding observed values in experimental trials.

Results: We show that the rates of walking and flying disperser production on leaves were the most important traits determining the fitness criteria, whereas dispersal distance and the clustering of flying dispersers on the target plant had no effect. We further show that the effect of dispersal parameters on aphid fitness depended strongly on plant characteristics.

Conclusion: Parameters defining the dispersal strategies of aphids at a local scale are key components of the fitness of these insects and may thus be essential in the adaptation to agricultural environments that are structured in space and time. Moreover, the fact that the effect of dispersal parameters on aphid fitness depends strongly on plant characteristics suggests that traits defining aphid dispersal strategies may be a cornerstone of host-plant specialization.

Show MeSH

Related in: MedlinePlus

Effect of dispersal parameters on fitness criteria in the case of a cucumber crop. Changing the plant parameters: effect of varying walking (Aw, Bw) and flying (Af, Bf) disperser aphid production parameters on the maximum number of aphids observed in the greenhouse (nmax, solid lines) and the production of propagules (nprop, doted lines) in the case of a cucumber crop. Arrows indicate the experimentally observed values of the parameters in a melon crop. Half error bars represent the standard deviation obtained from the 10 simulations of each point.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC1622755&req=5

Figure 5: Effect of dispersal parameters on fitness criteria in the case of a cucumber crop. Changing the plant parameters: effect of varying walking (Aw, Bw) and flying (Af, Bf) disperser aphid production parameters on the maximum number of aphids observed in the greenhouse (nmax, solid lines) and the production of propagules (nprop, doted lines) in the case of a cucumber crop. Arrows indicate the experimentally observed values of the parameters in a melon crop. Half error bars represent the standard deviation obtained from the 10 simulations of each point.

Mentions: When considering the discrepancy between observed and optimal values of the parameters of flying disperser production, it should be borne in mind that the NM1 clone of A. gossypii is specialized for host plants of the cucurbit family [45,46]. Cultivated species of this family, such as zucchini, cucumber and melon plants, grow rapidly and have a large carrying capacity for A. gossypii, which is the only aphid pest of these crops. However, this carrying capacity differs considerably between the plant species of this family, with large cucumber leaves able to support more than 10,000 aphids each [47]. We roughly evaluated the optimality of disperser production parameters for cucumber plants by running sets of simulations similar to those for melon plants, but setting the leaf carrying capacity parameter K to 70,000 and the resource depletion parameter KK to 5 (see methods, eq. 3). These values produced a population dynamics curve at the leaf scale similar to the previous curve, but with a maximum number of aphids close to 10,000 (data not shown). As shown in Fig. 3 for simulated melon crops, Fig. 5 shows the values of both fitness criteria when each of the four dispersal parameters were varied individually, the other three parameters being set to the values estimated from Experiment 1. The optimal values of the parameters for walking disperser production in melon crops were also almost optimal for cucumber crops, except that walking dispersal conferred neither an advantage nor a disadvantage for clonal fitness: neither of these fitness criteria was lower for Aw = 0 than for Aw > 0. However, the observed values of Af and Bf, which were far from optimal for flying disperser production in melon crops, were almost optimal for cucumber. Moreover, whatever the parameter values used, the "cucumber" simulations gave much larger numbers of aphids and propagules than the "melon" simulations. This suggests that: (1) the disperser production traits of genotypes of A. gossypii specialized on cucurbit plants are adapted to the host plant, increasing aphid fitness, as on cucumber plants, in terms of local density or large-scale dispersal; and (2) the parameters with the greatest power for selection are those determining the density-dependent production of flying dispersers. Moderate, density-independent walking dispersal may confer a selective advantage when the resource is not optimal.


Dispersal strategies of phytophagous insects at a local scale: adaptive potential of aphids in an agricultural environment.

Lombaert E, Boll R, Lapchin L - BMC Evol. Biol. (2006)

Effect of dispersal parameters on fitness criteria in the case of a cucumber crop. Changing the plant parameters: effect of varying walking (Aw, Bw) and flying (Af, Bf) disperser aphid production parameters on the maximum number of aphids observed in the greenhouse (nmax, solid lines) and the production of propagules (nprop, doted lines) in the case of a cucumber crop. Arrows indicate the experimentally observed values of the parameters in a melon crop. Half error bars represent the standard deviation obtained from the 10 simulations of each point.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1622755&req=5

Figure 5: Effect of dispersal parameters on fitness criteria in the case of a cucumber crop. Changing the plant parameters: effect of varying walking (Aw, Bw) and flying (Af, Bf) disperser aphid production parameters on the maximum number of aphids observed in the greenhouse (nmax, solid lines) and the production of propagules (nprop, doted lines) in the case of a cucumber crop. Arrows indicate the experimentally observed values of the parameters in a melon crop. Half error bars represent the standard deviation obtained from the 10 simulations of each point.
Mentions: When considering the discrepancy between observed and optimal values of the parameters of flying disperser production, it should be borne in mind that the NM1 clone of A. gossypii is specialized for host plants of the cucurbit family [45,46]. Cultivated species of this family, such as zucchini, cucumber and melon plants, grow rapidly and have a large carrying capacity for A. gossypii, which is the only aphid pest of these crops. However, this carrying capacity differs considerably between the plant species of this family, with large cucumber leaves able to support more than 10,000 aphids each [47]. We roughly evaluated the optimality of disperser production parameters for cucumber plants by running sets of simulations similar to those for melon plants, but setting the leaf carrying capacity parameter K to 70,000 and the resource depletion parameter KK to 5 (see methods, eq. 3). These values produced a population dynamics curve at the leaf scale similar to the previous curve, but with a maximum number of aphids close to 10,000 (data not shown). As shown in Fig. 3 for simulated melon crops, Fig. 5 shows the values of both fitness criteria when each of the four dispersal parameters were varied individually, the other three parameters being set to the values estimated from Experiment 1. The optimal values of the parameters for walking disperser production in melon crops were also almost optimal for cucumber crops, except that walking dispersal conferred neither an advantage nor a disadvantage for clonal fitness: neither of these fitness criteria was lower for Aw = 0 than for Aw > 0. However, the observed values of Af and Bf, which were far from optimal for flying disperser production in melon crops, were almost optimal for cucumber. Moreover, whatever the parameter values used, the "cucumber" simulations gave much larger numbers of aphids and propagules than the "melon" simulations. This suggests that: (1) the disperser production traits of genotypes of A. gossypii specialized on cucurbit plants are adapted to the host plant, increasing aphid fitness, as on cucumber plants, in terms of local density or large-scale dispersal; and (2) the parameters with the greatest power for selection are those determining the density-dependent production of flying dispersers. Moderate, density-independent walking dispersal may confer a selective advantage when the resource is not optimal.

Bottom Line: The spread of agriculture greatly modified the selective pressures exerted by plants on phytophagous insects, by providing these insects with a high-level resource, structured in time and space.The life history, behavioural and physiological traits of some insect species may have evolved in response to these changes, allowing them to crowd on crops and to become agricultural pests.Dispersal, which is one of these traits, is a key concept in evolutionary biology but has been over-simplified in most theoretical studies.

View Article: PubMed Central - HTML - PubMed

Affiliation: Unité de Lutte Biologique, INRA, 06903 Sophia-Antipolis, France. lombaert@antibes.inra.fr

ABSTRACT

Background: The spread of agriculture greatly modified the selective pressures exerted by plants on phytophagous insects, by providing these insects with a high-level resource, structured in time and space. The life history, behavioural and physiological traits of some insect species may have evolved in response to these changes, allowing them to crowd on crops and to become agricultural pests. Dispersal, which is one of these traits, is a key concept in evolutionary biology but has been over-simplified in most theoretical studies. We evaluated the impact of the local-scale dispersal strategy of phytophagous insects on their fitness, using an individual-based model to simulate population dynamics and dispersal between leaves and plants, by walking and flying, of the aphid Aphis gossypii, a major agricultural pest, in a melon field. We compared the optimal values for dispersal parameters in the model with the corresponding observed values in experimental trials.

Results: We show that the rates of walking and flying disperser production on leaves were the most important traits determining the fitness criteria, whereas dispersal distance and the clustering of flying dispersers on the target plant had no effect. We further show that the effect of dispersal parameters on aphid fitness depended strongly on plant characteristics.

Conclusion: Parameters defining the dispersal strategies of aphids at a local scale are key components of the fitness of these insects and may thus be essential in the adaptation to agricultural environments that are structured in space and time. Moreover, the fact that the effect of dispersal parameters on aphid fitness depends strongly on plant characteristics suggests that traits defining aphid dispersal strategies may be a cornerstone of host-plant specialization.

Show MeSH
Related in: MedlinePlus