1. Genetic modification of host acceptance by a seed beetle:
quasi-natural vs. artificial selection
Meagan Bridges, Jake Jones, AmberLeigh Muller & Frank Messina, Dept. of Biology, Utah State University
Introduction
Many plant-feeding insects use a fairly well-defined set of hosts, but are occasionally observed on an atypical host. The seed beetle Callosobruchus maculatus infests several grain legumes, especially Vigna spp. It has rarely been reported to attack lentil, a distant relative of its typical hosts (Credland, 1987). In three previous mass-selection experiments, we showed that larval survival in lentil increased rapidly after a bottleneck, from <2% to >70% in only 5-7 generations.
Host shifts by insects may also require modification of egg-laying behavior. Initial assays confirmed that most C. maculatus females fail to recognize lentil as a potential host. We used both quasi-natural and artificial-selection experiments to estimate the potential rate of change of host acceptance.
Newly emerged, isolated pairs kept on lentils for 3 d
Select pairs w/ 0 eggs
Assay F1
progeny on lentil
Unselected progeny
form next generation
Pairs kept on lentils for 3 d
Select pairs w/ most eggs
Generation
Assay F3 progeny on lentil and mung
Selection Protocol F1 F0 F2 F3
In the artificial-selection experiments, Acceptance (A) lines were established with females that laid eggs on lentil within 3 days; Rejection (R)-line females laid no eggs. In assays of F3 progeny, A females laid more than three times as many eggs on lentil as R females (Fig. 2), and only 27% of R females laid any eggs at all. The A and R selection lines did not differ in acceptance of mung bean.
Successful selection for greater acceptance of lentil had no effect on larval survival, i.e., there was no evidence of pleiotropy among genes affecting female behavior and those affecting larval performance.
Acceptance line
Rejection line
Eggs per female (+ SE)
27% laid
eggs
59% laid
Lentil Mung bean 5 10 15 20 25 30
Fig. 2
Test host
mung bean
lentil
Callosobruchus maculatus
Quasi-natural selection involves shifting replicate lines to a novel environment (host) and periodically comparing various traits in these lines with lines maintained in the ancestral environment. Any evolutionary change results from inherent variation in adaptedness to the new environment (Fry, 2003). Our quasi-natural experiment compared host acceptance between control lines (M, mung bean) and three lines switched to lentil (L1-3) for 5-20 generations.
Artificial selection involves measuring a particular trait in each generation, and using it to determine which individuals will serve as parents of the next generation. Two bidirectional experiments exposed >600 pairs of newly-emerged, M-line beetles to lentils for 3 days. New lines were established with pairs showing very high or low host acceptance (see Selection Protocol).
The three L lines independently evolved increased acceptance of lentil in <10 generations, although lentil was still accepted far less than mung bean (Table 1). Increased oviposition on lentil by the L lines had no effect on acceptance of mung bean. In a time-course experiment, both L and M females laid few or no eggs on lentil during the first 24 h of exposure, but many L females had laid several eggs by day two (Fig. 1).
Conclusions
Genetic modification of egg-laying behavior was not as dramatic as the increase in larval survival, but both kinds of selection experiments demonstrated heritable variation in the tendency to accept lentil.
Adaptation to lentil had no effect on the rate of acceptance of the ancestral host, mung bean.
Current research is examining whether rapid adaptation to lentil leads to cross-adaptation to other marginal hosts, or to changes in fitness components not directly related to host use (e.g., Messina, 2004).
L1 line (F15)
M line
Number of eggs (+ SE)
Days exposed to lentil seeds
Fig. 1
Table 1. Number of eggs (± SE) laid by L-line and M-line beetles on lentil or mung bean seeds
Test host
Line Lentil Mung bean
F ± ± 1.6
M ± ± 1.4
F ± ± 1.4
M ± ± 1.3
F ± ± 1.5
M ± ± 1.3
(N = ♀/ treatment; L lines had been reverted to mung bean for a generation).
References
Credland, P.F Effects of host change on fecundity and development of an unusual strain of Callosobruchus maculatus (F.) (Coleoptera: Bruchidae). J. Stored Prod. Res. 23:91-98.
Fry, J.D Detecting ecological trade-offs using selection experiments. Ecology 84:
Messina, F.J Predictable modification of body size and competitive ability following a host shift by a seed beetle. Evolution 58: