Progress 07/01/08 to 06/30/13
Outputs
Target Audience: Target Audience The primary audience for this work includes other agricultural scientists interested in what determines the diet breadth of pest insects, as well as basic scientists interested in mechanisms that promote or retard the process of adaptation to novel environments. As Callosobruchus maculatus is one of the most important stored-product pests in the world (but especially in Africa and Asia), understanding the beetle's host range (and its evolution) is of interest wherever stored grain legumes are vulnerable. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided? Opportunities Because the seed beetle Callosobruchus maculatus is a stored-product pest that has long been adapted to human stores of grain legumes, the laboratory provides an exceptionally close approximation of its "natural" habitat. Moreover, this highly tractable system allows students to gather significant amounts of data in short periods of time, and participate in an experiment from start to finish, from data collection to analysis to publication. Sixteen undergraduates have gained valuable research experience in our lab during the duration of this project, and ten of them were involved in the construction of scientific posters (as part of the requirements for obtaining formal course credits in Undergraduate Research). Of the 13 peer-reviewed publications that appeared during this funding period, undergraduates served as one or more co-authors on seven of them. Because of our long-term collaboration with Dr. Charles Fox at the University of Kentucky (who served as a co-author on several papers published during this funding period), our joint research efforts have also provided training opportunities at his institution. Further student opportunities are listed in the Dissemination section. How have the results been disseminated to communities of interest? Dissemination The results of our experiments have mainly been disseminated through publication in peer-reviewed scientific journals and through oral or poster presentations at scientific meetings. Ten undergraduates were involved in presenting local posters of the research supported by this project. We published 13 peer-reviewed papers between 2008 and 2013. Our work and these publications have also generated interest from other labs studying the process by which insects adapt to new host plants. In the middle of this funding period, we established a new collaboration with a DNA sequencing laboratory at Notre Dame (headed by Dr. Jeff Feder). Two graduate students and a post-doc in this lab have obtained samples of our lines for sequencing and analysis, and have already made substantial progress. In addition, our selection lines have recently been transferred to graduate students at Rice University (Michelle Downey) and Cornell University (Kristin Hook). After reading about our work, these students decided to adopt seed beetles as a model system for answering questions in behavior and evolution, and we have spent significant time consulting with them about the development of their projects. What do you plan to do during the next reporting period to accomplish the goals? Plan of Work This project ended on June 30, 2013.
Impacts
What was accomplished under these goals?
Accomplishments Our research was aimed at understanding the processes by which insects adapt to new host plants, which can lead to the establishment of new agricultural pests. The first objective was to use quantitative-genetic analyses to establish the genetic architecture underlying rapid adaptation to a new crop plant. We used line crosses to show that there are both additive and non-additive (dominance and epistasis) factors that mediate rapid adaptation to lentil in terms of larval performance (larval survival in lentil rose from 1% to >90% in less than 30 generations). Similar crosses showed that a second component of adaptation, increased egg-laying on lentil, was inherited in a largely additive fashion. This work is currently being followed up in a new project that will use next-generation sequencing to identify specific genes responsible for these inheritance patterns. Our second objective sought to determine whether adaptation to a poor host affects the suitability of other marginal hosts or non-hosts, i.e., whether there is cross-adaptation to hosts never encountered. We found little evidence for cross-adaptation, which means that we do not expect a broader host-range expansion. This work used only a single mung bean line and lentil line, however. We are now expanding the work to get a more robust answer to whether cross-adaptation is likely, particularly because it would increase the destructiveness of the insect pest. Our third objective was to determine whether adaptation to a novel host involves genetic trade-offs, so that increased performance on the novel host simultaneously leads to poorer performance on the ancestral host. Experiments to date show little or no evidence of a trade-off: three independent lines adapted to lentil still retain high performance on the ancestral host, mung bean. This implies that changes in gut enzymatic activity that permit dramatically improved performance in lentil does not reduce growth rate, adult size, or survival on mung bean. Consequently, genetic trade-offs are not a general explanation for the narrow diets of herbivorous insects. We are currently conducting reversion experiments as an alternative way to detect trade-offs. The fourth objective examined the importance of non-genetic effects on insect performance on a novel host. We specifically wanted to know if parental rearing host affected offspring performance, which can occur in a variety of ways, including epigenetic modification of the offspring genome. Our experiments showed conclusively that there is little or no effect of parental environment on either larval performance in seeds or the egg-laying preferences of females. Our final objective was to determine whether different geographic populations of seed beetles differ in their rate of adaptation to a novel host, mainly because they differ in the amount and kind of standing genetic variation needed for rapid adaptation. We showed that both African and Asian populations of beetles rapidly adapted to a host of moderate quality (adzuki bean), which implies that beetle populations routinely possess enough the necessary standing genetic variation. However, the magnitude of the response was greater in the African population, which was initially less well-adapted to adzuki bean.
Publications
- Type:
Journal Articles
Status:
Published
Year Published:
2013
Citation:
Fox, C. W., Messina, F. J. (2013). Life History. Oxford Bibliographies in Ecology. http://www.oxfordbibliographies.com/view/document/obo-9780199830060/obo-9780199830060-0016.xml
- Type:
Journal Articles
Status:
Published
Year Published:
2013
Citation:
Messina, F. J., Durham, S. L. (2013). Adaptation to a novel host by a seed beetle (Coleoptera: Chrysomelidae: Bruchinae): effect of source population. Environmental Entomology, 42, 733-742.
- Type:
Journal Articles
Status:
Published
Year Published:
2013
Citation:
Messina, F. J., Morris, B. D., Fox, C. W. (2013). Effect of inbreeding on host discrimination and other fitnes components in a seed beetle. Annals of the Entomological Society of America, 106, 128-135..
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Progress 01/01/12 to 12/31/12
Outputs
OUTPUTS: "In 2012 we conducted research aimed at understanding genetic and ecological interactions between insects and their crop hosts. A cosmopolitan beetle pest was used as a model system because it is well known to form "biotypes" that differ in their host ranges. With several undergraduate participants, we continued selection experiments to understand the genetic basis and potential trade-offs associated with adaptation to a marginal host. Previous work showed that laboratory selection can increase beetle survival on lentil cultivars from 1% to >90% in fewer than 30 generations, and the tendency to lay eggs on this host can increase two- to three-fold. We first used line crosses to establish the mode of inheritance underlying this radical host shift, and these results were disseminated in a 2012 paper that demonstrated additive inheritance of evolved differences in egg-laying behavior. We are now conducting reversion experiments to examine potential trade-offs, as would be expected if genotypes that are optimal on the novel host are simultaneously sub-optimal on the ancestral host. Lines that are well adapted to the novel host are reverted back to the ancestral host and will be tested to see whether there is a loss of adaptation after a number of generations. To understand the molecular-genetic basis of adaptation to an initially poor host (lentil), our lines are being examined with next-generation sequencing techniques in the lab of Dr. Jeff Feder at the University of Notre Dame. As background work, we conducted family crosses to establish RAD tags (Restriction site Associated DNA markers) to guide the search of the genetic changes underlying adaptation. Two other projects involved collaboration with Dr. Charles W. Fox at the University of Kentucky. One project, which also resulted in a publication in 2012, investigated seed-beetle effects on non-crop hosts in Arizona. This study examined whether seed beetles have positive effects (via scarification and improvement of germination) or negative effects for two desert legumes used in restoration of degraded arid lands. A second project examined whether egg-laying behavior in pest seed beetles is modified by inbreeding. Inbreeding often has unpredictable effects on fitness-related traits in insects, but little is known about effects on behavior. We used a "block design" in a large-scale experiment that measured egg-laying behavior. A PYTHON-language program was written by USU undergrad Benjamin Morris to score how inbred and outbred females differ in their ability to detect whether legume seeds are already occupied. This work will be published in 2013. One other lab is already using our program to measure oviposition behavior, and the program will be generally available. USU undergrad Jason Muelleck presented this work at the Biology Department Undergraduate Research Symposium in November 2012. PARTICIPANTS: Dr. Charles W. Fox and his colleagues in the Department of Entomology at the University of Kentucky collaborated on the investigation of wild seed beetles and their effects on desert legumes, and conducted the final analyses of the inbreeding experiment. Selection lines that have diverged in their ability to use a novel host were shipped to Dr. Jeff Feder at the University of Notre Dame, and DNA extractions in his lab have been sent off for next-generation sequencing to compare the lentil and mung-bean lines. Our work in 2012 involved five USU undergraduates: Benjamin Morris, Nicole Pena, Chelsea Christensen, Chelsea Hole, and Jason Muelleck. Benjamin Morris wrote the Python-language program needed to automate the analysis of oviposition behavior in >1400 females. He is now a graduate student in Computer Science in North Carolina. In addition, two Logan High School students, Paisley Tarboton and Ryan Kobe, helped with the data collection in the inbreeding experiment. Nicole Pena was a co-author on a paper published in September 2012. Statistical consulting for some of our projects has been provided by Susan Durham, the statistician for the Ecology Center at USU. TARGET AUDIENCES: The primary audience for this work is mainly other agricultural scientists interested in what determines the diet breadth of pest insects, as well as basic scientists interested in mechanisms (particulary at the genomic level) that promote or retard the process of adaptation to novel environments. As Callosobruchus maculatus is one of the most important stored-product pests in the world (but especially in Africa and Asia), understanding the beetle's host range (and its evolution) is of interest wherever stored grain legumes are vulnerable. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
Changes in knowledge: Because insect populations are notorious for occasionally colonizing new crop hosts - hosts that not previously been considered within the host range of a given insect - it is important to understand factors that promote or retard such host shifts. We have relatively little understanding of the formation of novel pest biotypes that can attack crops usually resistant to that insect species. Our work provides knowledge regarding both ecological and genetic factors involved in an insect's expansion of its host range. We also provide additional knowledge with respect to the relative importance of changes in adult behavior (egg-laying females) vs. larval physiology (feeding efficiency and larval survival). This type of information is poorly known at the level of the candidate genes involved, particularly in species other than Drosophila. The genetic basis of adaptation is often difficult to determine because host shifts may not be recognized until well after they occur, and divergent populations have experienced different environments in addition to different hosts. By performing experimental evolution in the laboratory, we examined the basis of rapid evolution via line crosses between lines adapted to a novel host vs. lines maintained on the ancestral host. Crosses examining larval performance (survival, development time, and body mass) and egg-laying behavior demonstrated that adaptation to an initially poor host involves both additive and non-additive genetic components. If cross-adaptation occurs, then a shift to a very different host may significantly expand a pest insect's host range, and formerly resistant hosts may become susceptible. If the planned genome scans are successful, we should be able to isolate candidate genes responsible for both improved larval performance and increase host acceptance. The seed beetle-grain legume association can therefore serve as a well-controlled model system for understanding plant-pest interactions.
Publications
- Fox, C. W., Wallin, W. G., Bush, M. L., Czesak, M. E., & Messina, F. J., (2012). Effects of seed beetles on the performance of desert legumes depend on host species, plant stage, and beetle density.: Journal of Arid Environments, 80: 10-16. (Published).
- Messina, F. J., & Pena, N. M., (2012). Mode of inheritance of increase host acceptance in a seed beetle.: Bulletin of Entomological Research, 102: 497-503. (Published).
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Progress 01/01/11 to 12/31/11
Outputs
OUTPUTS: We continued in 2011 to examine the evolution of interactions between insects and both crop and non-crop hosts. We use seed beetles as a model system because different geographic populations are well-known to have different host ranges, and therefore differ in their abilities to attack grain-legume hosts. Our main activities in 2011 were to continue selection experiments that mimicked host shifts in nature or in agricultural systems. We finalized our analyses of the mode of inheritance of variation in larval performance on novel and ancestral legume crops. This analysis involved a series of line crosses between beetle populations that were maintained on the ancestral host (and show 1% survival on the novel host) and lines selected on the novel host (which show >90% survival after 20 generations). We then focused on line crosses to determine the basis by which female seed beetles increase host acceptance, i.e., an increased tendency to lay eggs on the novel and initially less preferred host. Dissemination of the results of our selection experiments involved one paper published in May 2011 that demonstrated both additive and non-additive genetic components underlying differences in larval performance between adapted and non-adapted lines. A second paper analyzing the inheritance of egg-laying behavior between adapted and non-adapted lines is currently submitted and in review. We recently sent our selection lines to the lab of Dr. Jeff Feder at the University of Notre Dame, who intends to initiate genomic analyses to understand the molecular basis of rapid adaptation to novel hosts by pest insects. Dr. Feder and his colleagues intend to establish RAD tags (Restriction site Associated DNA markers) for seed beetles. Once RAD tags have been isolated, they can then be used to isolate DNA sequence polymorphisms associated with the non-adapted (ancestral) and adapted lines. Other activities involved two collaborations with Dr. Charles W. Fox at the University of Kentucky. One project examined whether the tendency to accept a novel crop host could be predicted by the beetle's tendency to "dump" eggs when females are deprived of hosts. These results were disseminated in a paper published in May 2011. A second project investigated seed-beetle effects on non-crop hosts in Arizona. This study examined whether seed beetles have positive effects (via scarification and improvement of germination rates) or negative effects (by consuming so much tissue as to kill the seed) for two dominant desert legumes that are used in restoration of degraded aridland habitats. A final activity was serving as the editor of a special issue of the journal Functional Ecology, one of the journals of the British Ecological Society. As I ended a six-year stint as editor for this journal, I wrote an introduction for a special Virtual Issue on the Evolutionary Ecology of Mutualisms, and compiled an issue of 17 papers that focuses on mutualistic interactions between species. This Introduction and issue were advertised and available on the journal website and that of Wiley Interscience. PARTICIPANTS: Analyses of line crosses, investigation of egg-dumping behavior, and demonstrating the impacts of seed beetles on wild desert legumes were all conducted in collaboration with Dr. Charles W. Fox in the Department of Entomology at the University of Kentucky. Selection lines that have diverged in their ability to use a novel host were shipped to Dr. Jeff Feder at the University of Notre Dame but no sequencing data are yet available. Individuals who have worked on the project in 2011 include four undergraduates: Nicole Pena, Chelsea Christensen, Bryant Loosle, and Jason Muelleck. All four plan to continue part-time in 2011. Nicole Pena is a co-author on a paper currently in review, and C. Christensen will be a co-author on a paper submitted in 2012.. Six other undergraduates served as temporary volunteers for one week in August, when a large-scale experiment required a lot of work. TARGET AUDIENCES: The primary audience for this work includes other agricultural scientists interested in what determines the diet breadth of pest insects, as well as basic scientists interested in mechanisms that promote or retard the process of adaptation to novel environments. As Callosobruchus maculatus is one of the most important stored-product pests in the world (but especially in Africa and Asia), understanding the beetle's host range (and its evolution) is of interest wherever stored grain legumes are vulnerable. PROJECT MODIFICATIONS: Not relevant to this project.
Impacts
Changes in knowledge: The genetic basis by which insects are able to expand their host ranges is poorly known, but these mechanisms frequently allow insect populations to attack crops previously considered resistant to the insect. This is particularly true for non-Drosophila, pest species. The genetic basis of adaptation is often difficult to determine because host shifts may not be recognized until well after they occur, and divergent populations have experienced different environments in addition to different hosts. By performing experimental evolution, we examined the genetic basis of rapid evolution via line crosses between lines adapted to a novel host vs. lines maintained on the ancestral host. Crosses examining larval performance (survival, development time, and body mass) demonstrated that adaptation to an initially poor host involves both additive and non-additive genetic components. For host acceptance (egg-laying behavior), available evidence from line crossed indicated purely additive inheritance, as hybrids accepted the novel host at a rate intermediate to the adapted and non-adapted (ancestral) lines. The degree of additivity of these traits and the number of genes involved are both relevant to the likelihood of fixation of near fixation of alleles that permit an expansion of the pest's host range. As this pest insect's genome becomes better characterized, we anticipate being able to isolate specific candidate genes responsible for both improved larval performance and increase host acceptance, possibly in collaboration with Dr. Jeff Feder's lab at the University of Notre Dame. The resulting information can be used to help explain why some pests (or certain pest populations) maintain narrow host ranges, while others often incorporate new crops in their diet. Our collaboration with Dr. Charles Fox at the University of Kentucky showed that different seed beetle populations (biotypes) can have substantially different impacts on host seeds. The tendency to colonize a new legume host is not a simple function of oviposition specificity or egg-dumping behavior. Finally, the work with wild seed beetles demonstrated that seed-beetle effects on non-crop hosts can be highly unpredictable and varies as a function of host species, plant stage, and beetle density.
Publications
- UTAO+0578 Messina, F. J., (2011). Introduction. Virtual Issue: The Evolutionary Ecology of Mutualisms: Functional Ecology. (Published).
- UTAO+0578 Messina, F. J., & Fox, C. W., (2011). Egg-dumping behavior is not correlated with wider host acceptance in the seed beetle Callosobruchus maculatus (Coleoptera: Chrysomelidae: Bruchinae).: Annals of the Entomological Society of America, 104: 850-856. (Published).
- UTAO+0578 Messina, F. J., & Jones, J. C., (2011). Inheritance of traits mediating a major host shift by a seed beetle, Callosobruchus maculatus (Coleoptera: Chrysomelidae: Bruchiae).: Annals of the Entomological Society of America, 104: 808-815. (Published).
- UTAO+0578 Fox, C. W., Wagner, J.D., Cline, S., Thomas, F.A., & Messina, F. J., (2011). Rapid evolution of lifespan in a novel environment: sex-specific responses and underlying genetic architecture.: Evolutionary Biology, 38: 182-196. (Published).
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Progress 01/01/10 to 12/31/10
Outputs
OUTPUTS: We continued to investigate processes involved in host shifts by herbivorous insect pests. We have ongoing selection experiments in which lines shifted to new legume hosts are periodically assayed for adaptive responses in a variety of traits. Our model organism is the cowpea seed beetle, Callosobruchus maculatus, a serious pest of many of the world's most important grain legumes. Different geographic populations of this insect have been reported to have different host ranges and we use experimental evolution to understand rapid changes in the beetle's host range. We performed and analyzed line crosses to determine the inheritance of traits that have diverged in lines shifted to a novel host. Larval survival in lentil was initially 1%, but, after a severe population bottleneck, three mass-selection experiments produced lines with >80% survival in <20 generations. We performed crosses between each lentil-adapted line (L1-3) and the mung-bean line (M) from which they were independently derived. Survival in lentil was highly divergent between parental lines: >90% in each L line vs. 0% in the M line. Survival of reciprocal F1 and F2 progeny indicated largely additive (intermediate) inheritance, with a small dominance deviation toward the M-line (in the L1 cross) or L-line (in the L2 and L3 crosses), and no evidence of sex-linkage or cytoplasmic effects. In a second set of crosses, progeny from backcrosses to the M line survived at a lower rate than expected by pure additivity. One explanation for this result is that successful development in lentil is influenced by multiple loci, and a threshold of enzymatic activity is needed to overcome seed toxins. Additive inheritance of initially rare alleles (as standing genetic variation) helps explain repeatable, rapid adaptation to a marginal host. We now turn our attention to the inheritance of the second key trait: the behavior of egg-laying females. We have performed crosses between three separate lentil-adapted lines and the ancestral, mung-bean line from which they were independently derived. These data are now being collected. We hope to establish collaborations that will foster genomic analyses to identify candidate genes involved in radical host shifts. Our work was mainly disseminated in 2010 in two publications. One of these papers (in collaboration with Dr. Charles Fox at the University of Kentucky) demonstrated that genetic differences among beetle populations in how they attack their seed hosts translates into very different levels of damage to seeds. Thus, one cannot develop simple economic threshold models at the species level if similar densities of beetle larvae have very different effects on seed germination rates and seedling growth. The primary target audience for this work includes agricultural scientists interested in the susceptibility of grain legumes, as well as biologists generally interested in the genetics underlying adaptation to novel environments. PARTICIPANTS: Some of the line crosses and selection experiments have been analyzed with the collaboration of Dr. Charles W. Fox in the Department of Entomology at the University of Kentucky. Individuals who have worked on the project in 2010 include rwo underergraduate students: J Tasha Cosgrove and Nicole Pena. Each of these students have provided sufficient input so as to be included as co-authors on future publications. Co-authored publications with Dr. Fox involved three additional undergraduates who assisted in the experiments conducted at the University of Kentucky. TARGET AUDIENCES: The primary audience for this work includes other agricultural scientists interested in what determines the diet breadth of pest insects, as well as basic scientists interested in mechanisms that promote or retard the process of adaptation to novel environments. As Callosobruchus maculatus is one of the most important stored-product pests in the world (but especially in Africa and Asia), understanding the beetle's host range (and its evolution) is of interest wherever stored grain legumes are vulnerable. PROJECT MODIFICATIONS: There are no planned modifications to this project.
Impacts
Changes in knowledge: Because the basis by which insects adapt to novel plants is poorly known, our experiments contribute to a better and more mechanistic understanding of how pest insects can rapidly colonize a novel host - a phenomenon that is commonly observed when a crop is introduced into a new geographic region. Our experiments established that pest populations contain standing genetic variation in the form of rare alleles that are inherited in a largely additive fashion. Classical genetic models have shown that, with additive inheritance, a population can show rapid fixation or near fixation of alleles that permit a pest to expand its host range. Despite the large number of instances of pest insects observed to colonize a new crop, there has been little previous research to document the genetic changes that accompany host-range expansions. Most studies have been limited to populations or closely related species that have long diverged in their host ranges. We examined the inheritance of traits mediating rapid adaptation to an extremely poor host by the seed beetle Callosobruchus maculatus. Now that this insect's genome is becoming better known, it should be possible to identify specific genes that mediate the formation of new "host races." This sort of information can be used to help explain why some pests maintain relatively narrow and predictable host ranges, and others are routinely able to incorporate new crops into their diet, and hence cause the need for new pest management strategies. The results of our studies are generally relevant to other interactions between insect pests and novel host plants, and we hope that the C. maculatus-grain legume interaction can become an even better model system for elucidating the mechanisms underlying plant/pest interactions. Our other, recently published collaboration with Dr. Charles Fox has shown that different populations of the same pest insect can attack the a given host in different ways, and hence inflict different levels of damage - even at the same pest densities. Thus, our research raises an important cautionary note in attempts to establish economic thresholds or damage indices at the pest species level. For a cosmopolitan pest that has undergone signficant levels of genetic differentiation among geographic populations, economic impacts may have to be quantified at the local level and tailored to individual populations. In general, our research shows that there are economic consequences to the well-know ability of insects to show local adaptation and the formation of different biotypes within a species.
Publications
- Messina, F. 2010. Allocating Eggs Among Multiple Hosts By Parasitic Insects. In: Evolutionary Behavioral Ecology, Oxford University Press, New York, NY. pg. 180-182.
- Messina, F. 2010. Biotypes of the seed beetle Callosobruchus maculatus have differing effects on the germination and growth of their legume hosts. Agricultural and Forest Entomology, Oxford, United Kingdom 12:353-362. DOI: 10.1111/j.1461-9563.2010.00484.x.
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Progress 01/01/09 to 12/31/09
Outputs
OUTPUTS: Our experiments in 2009 continued to elucidate the mechanisms and consequences of host shifts by herbivorous insects. We made great progress in performing selection experiments to understand the processes that permit pest insects to attack new crops or cultivars. Our model system is the seed beetle Callosobruchus maculatus, which is a serious pest of many of the world's most important grain legumes, particularly in Asia and Africa. Interfertile populations of this species sometimes show striking differences in the hosts they are able to attack, as well as in many behavioral, physiological, and life-history traits. Some grain legumes are quite marginal hosts, such that the beetle is only rarely reported to sustain populations on these hosts. Our protocols allow us to investigate genetic changes in key traits that permit colonization of a formerly unsuitable host, as has happened in certain parts of this insect's geographic range. We routinely use both quasi-natural and artificial-selection, as well as line crosses between populations or selection lines that have diverged with respect to their ability to attack a particular type of legume. The results are generally relevant to understanding plant-insect interactions, and have mainly been disseminated via four publications that appeared in 2009 as well as an additional paper that is in press. On some projects, we continue to work closely with Dr. Charles Fox at the University of Kentucky, who has conducted multiple crosses of our selection lines and subsequent data analyses. One publication that is in press has demonstrated how geographic variation in host use can lead to strong variation in larval behavior, which in turn significantly affects the degree of seed damage caused by a given larval density. Thus, our results have practical applications to economic threshold models for this pest. I have also sent samples of our lab strains to two other universities, with the hope that these lines will be especially useful when the C. maculatus genome becomes well known. The primary target audience for our results includes agricultural scientists interested in particular in seed beetle infestation of grain legumes, as well as biologists generally trying to understand the genetics of adaptation to novel environments. Because our selection experiments produced such a rapid expansion in the pest's host range, we are now attempting to establish a collaboration with a lab at the University of Nevada at Reno to perform genomic analyses and identify the major genes involved in the host shift. PARTICIPANTS: Line crosses and selection experiments described in the Plan of Work will be conducted and analyzed with the collaboration of Dr. Charles W. Fox in the Department of Entomology at the University of Kentucky. Individuals who have worked on the project in 2009 include four undergraduate students: Jake C. Jones (now at the U. of U. medical school), April Cowley, Tasha Cosgrove, and Nicole Pena. Three of these students have provided sufficient input so as to be included as co-authors on resulting publications. Co-authored publications with Dr. Fox involved three additional undergraduates who assisted in the experiments conducted at the University of Kentucky. TARGET AUDIENCES: The primary audience for this work includes other agricultural scientists interested in what determines the diet breadth of pest insects, as well as basic scientists interested in mechanisms that promote or retard the process of adaptation to novel environments. As Callosobruchus maculatus is one of the most important stored-product pests in the world (but especially in Africa and Asia), understanding the beetle's host range (and its evolution) is of interest wherever stored grain legumes are vulnerable. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
Scientific Advancement: Our experiments in 2009 greatly increased our understanding of the means by which the seed beetle Callosobruchus maculatus colonizes novel legume hosts. We have now established three independent selection lines that each show over 90% survival in lentil seeds, despite the fact that initial survival in the non-adapted, mung-bean line is less than two percent. The results demonstrated that the base population of the beetle contained rare alleles that permitted a rapid improvement in larval performance after an extreme population bottleneck. These results reflect standing genetic variation in key performance traits on lentil (survival to adult emergence, body mass, development time), but does not reveal the mode of inheritance of the ability to perform well in lentil. Inheritance patterns (degree of dominance vs. additivity, the role of epistasis, etc.) can greatly affect the rate of adaptation to any new environment (host). We therefore performed several line crosses between each of the three lentil lines and the ancestral line from which they were derived. We examined the rate at which beetle lines increase their oviposition on lentil. These experiments demonstrated that egg-laying behavior can be modified rapidly through either quasi-natural selection (in which replicate populations are simply transferred to the new environment) or artificial selection (in which short term assays of egg-laying behavior are used to select certain parents for each generation). Line crosses are being performed to compare the inheritance of increased adult oviposition with the inheritance of improved larval performance. Our current results suggest no correlation between the traits, which are free to evolve independently. Changes in both larval physiology and adult behavior were sufficient to convert lentil from an extremely poor host to a highly suitable one in <20 generations. We also examined whether rapid adaptation to one marginal host (lentil)leads to cross-adaptation to other poor hosts, including those that are closely related to the novel host. Few studies have assessed whether adaptation to a novel host involves mechanisms that have cross-over effects to other hosts. Cross-adaptation would occur, for example, if a newly evolved detoxification mechanism in the insect gut acted to improve larval performance in hosts that have not been encountered but contain similar toxins. The seed beetle-legume system is thus allowing us to address this general phenomenon, which could lead to insect "biotypes" that can attack a range of hosts that are usually resistant to the insect. A final objective of our experiments is to increase our knowledge of possible trade-offs associated with genetic adaptation to new hosts or environments. The specialized diets of insects have often been explained by invoking fitness trade-offs; continued adaptation to one host can simultaneously reduce performance on other hosts (which often present a very different array of physical and chemical characteristics). The overall impact of our research is therefore to answer address mechanisms underlying interactions between pests and their hosts.
Publications
- Messina, F. J., and Jones, J.C. 2009. Does rapid adaptation to a poor-quality host by Callosobruchus maculatus (F.) cause cross-adaptation to other legume hosts Journal of Stored Products Research 45:215-219.
- Messina, F.J., Mendenhall, M. and Jones, J.C. 2009. An experimentally induced host shift in a seed beetle. Entomologia Experimentalis et Applicata 132:179-187.
- Fox, C.W., Wagner, J.D., Cline, S., Thomas, F.A., and Messina, F.J. 2009. Genetic architecture underlying convergent evolution of egg-laying behavior in a seed-feeding beetle. Genetica 136:179-187.
- Messina, F.J., Jones, J.C., Mendenhall, M., and Muller, A. 2009. Genetic modification of host acceptance by a seed beetle, Callosobruchus maculatus (Coleoptera: Bruchidae). Annals of the Entomological Society of America 102:181-188.
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Progress 01/01/08 to 12/31/08
Outputs
OUTPUTS: We have continued our experiments aimed at understanding the processes that permit pest insects to attack new crops or cultivars. As a model system, we use a seed beetle that attacks many of the world's most important grain legumes. Some grain legumes are unsuitable, however, and the beetle is only occasionally reported to infest certain marginal hosts. Our protocols allow us to investigate genetic changes in key traits that permit colonization of a formerly unsuitable host. We routinely use both quasi-natural and artificial-selection experiments, as well as line crosses between populations or selection lines that have diverged with respect to their ability to attack a particular legume. The results are relevant to understanding plant-insect interactions in general, and have mainly been disseminated via three peer-reviewed publications in press for 2009 (and listed elsewhere) and presentations at national meetings. I presented much of our recent results during an invited departmental seminar at Idaho State University in April. On some projects, we continue to work closely with Dr. Charles Fox at the University of Kentucky, who has conducted multiple crosses of our selection lines and subsequent data analyses. I have also sent samples of our lab strains to two other universities. The primary target audience for our results includes agricultural scientists interested in particular in seed beetle infestation of grain legumes, as well as biologists generally trying to understand the genetics of adaptation to novel environments. PARTICIPANTS: Line crosses described in the Plan of Work will be conducted and analyzed with the collaboration of Dr. Charles W. Fox in the Department of Entomology at the University of Kentucky. Individuals who have worked on the project in 2008 include four undergraduate students: Jake C. Jones, AmberLeigh Muller, April Cowley, and Meagan Bridges. Three of these students have provided sufficient input so as to be included as co-authors on resulting publications. TARGET AUDIENCES: The primary audience for this work includes other agricultural scientists interested in what determines the diet breadth of pest insects, as well as basic scientists interested in mechanisms that promote or retard the process of adaptation to novel environments. As Callosobruchus maculatus is one of the most important stored-product pests in the world (but especially in Africa and Asia), understanding the beetle's host range (and its evolution) is of interest wherever stored grain legumes are vulnerable. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
Many of our experiments in 2008 produced new information on the means by which the seed beetle Callosobruchus maculatus colonizes novel legume hosts. One forthcoming publication investigated the rate at which larval survival, development time, and body size evolved on an extremely poor host, lentil, following mass selection. The results demonstrated that the base population of the beetle contained rare alleles that permitted a rapid improvement in larval performance after an extreme population bottleneck. These results were observed in all three mass-selection attempts and thus reflect standing genetic variation in key performance traits on lentil. A second publication demonstrated the more modest rate at which beetle lines increase their oviposition on lentil. These experiments demonstrated that egg-laying behavior can be modified rapidly in seed beetle populations through either quasi-natural selection (in which replicate populations are simply transferred to the new environment) or artificial selection (in which short term assays of egg-laying behavior are used to select certain parents for each new generation). Taken together, our results demonstrated that changes in both larval physiology and adult behavior in less than 20 generations were sufficient to convert lentil from a non-host (or extremely poor host) to a highly suitable host. Another set of experiments (described in a paper that is currently in review) examined whether rapid adaptation to one marginal host (lentil) leads to cross-adaptation to other poor hosts, including those that are closely related to the novel host. Few studies are available to assess whether adaptation to a novel host involves mechanisms that have carry-over effects to other hosts. Cross-adaptation would occur, for example, if a newly evolved detoxification mechanism in the insect gut acted to improve larval performance in hosts that have never been encountered but contain similar toxins. The seed beetle-legume system is allowing us to address this general phenomenon, which could lead to insect "biotypes" that can attack a range of hosts that are usually resistant to the insect. A final objective of our experiments is to increase our knowledge of possible trade-offs associated with genetic adaptation to new hosts or environments. The specialized diets of insects have often been explained by invoking fitness trade-offs; continued adaptation to one host can simultaneously reduce performance on other hosts (which often present a very different array of physical and chemical characteristics). By performing experimental evolution and assaying selection lines at regular intervals, we are able to compare insect performance between lines on both ancestral and novel hosts. We have consistently found a general lack of such trade-offs. There is therefore little penalty associated with a rapid host-range expansion. The overall impact of our research is therefore to answer some long-standing questions regarding the nature of interactions between insect pests and their hosts.
Publications
- Fox, C., Thompson, K, Cresswell, J., Messina, F. & Baker, L. 2008. Editorial. Functional Ecology 22:1-2.
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Progress 01/01/07 to 12/31/07
Outputs
OUTPUTS: Many insect pests are known to infest a fairly well-defined set of host plants, but are occasionally observed on an atypical crop host. We continued to conduct research on the processes that promote or contrain the ability of plant-feeding insects to shift to new or unusual crop hosts. We use as a model system the seed beetle Callosobruchus maculatus, which infests several grain legumes (especially Vigna spp.). It has rarely been reported to attack lentil, a distant relative of its typical hosts. In three mass-selection experiments using a mung-bean adapted population, we showed that larval survival in lentil increased rapidly after a population bottleneck, from less than 2% to more than 70% in 5-7 generations. After 20 generations, survival in lentil was indistinguishable from that in mung bean. Repeated adaptation to such a marginal host indicates that beetle populations harbor rare alleles permitting this particular host shift. A frequent explanation for the highly
specialized diets of herbivorous insects has been the possibility of trade-offs across hosts, i.e., adaptation to a new or unusual host causes a decrease in insect performance on the ancestral host. The only trade-off detected in our experiments was that beetles in lentil-adapted lines developed significantly more slowly within mung beans than beetles in mung bean lines did. Successful host shifts by insects may also require modification of egg-laying behavior. Preliminary experiments demostrated that many C. maculatus females do not recognize lentil as a potential host. We therefore used both quasi-natural and artificial-selection experiments to estimate the potential rate of change of acceptance of lentil for oviposition. In the former experiments, the lentil-adapted lines independently evolved increased acceptance of lentil in less than generations, although lentil was still accepted far less than mung bean. Increased oviposition on lentil by the lentil-adapted lines had no effect
on acceptance of mung bean. Two artificial-selection experiments also produced significant responses. Acceptance lines were established from females that laid the most eggs on lentil in a three-day assay; rejection lines females were established using females that laid no eggs. Among F3 progeny, acceptance-line females laid more than three times as many eggs on lentil as rejection-line females; only 27% of rejection-line females laid any eggs at all. The lines did not differ in their acceptance of mung bean, which again suggests that adaptation to the novel host did not affect the behavioral response to the ancestral one. Assays of F4 progeny revealed that successful selection for greater acceptance of lentil had no effect on larval survival, i.e., there was no evidence of pleiotropy among genes that affect female egg-laying behavior and those that affect larval performance within seeds. In general, modification of egg-laying behavior was not as dramatic as the increase in larval
survival, but both quasi-natural and artificial selection demonstrated heritable variation in beetle populations the tendency to accept lentil.
PARTICIPANTS: Line crosses described in the Plan of Work will be conducted and analyzed with the collaboration of Dr. Charles W. Fox in the Department of Entomology at the University of Kentucky.
TARGET AUDIENCES: The primary audience for this work includes other agricultural scientists interested in what determines the diet breadth of pest insects, as well as basic scientists interested in mechanisms that promote or retard the process of adaptation to novel environments.
PROJECT MODIFICATIONS: We anticipate no major changes in the final six months of this project.
Impacts
The seed beetle Callosobruchus maculatus is one of the most serious pests of stored grain legumes or pulses in the world. It inflicts heavy damage especially in countries where storage facilities are poor, pesticides are costly, and, at the same time, grain legumes are a critical source of protein. There is some ambiguity in scientific literature on the host range of this pest; some crops are reliably attacked by the insect in the storage environment, while others are rarely attacked. It is important to isolate the mechanisms by which a pest insect may incorporate a new host into its diet. We have summarized our research results in two posters presented at Annual Meetings of the Entomological Society of America (in 2006 and 2007), as well as at the National Conference for Undergraduate Research in 2007 at Dominican University. The results described in the Outputs section will be summarized in two publications in the coming year (we completed and published in 2007 two
papers with results from previous projects that used seed beetles for other research questions). One forthcoming paper will document the rate at which larval survival, development time, and body size can improve in a marginal host follwing repeated mass selection. A second will address the changes in egg-laying behavior needed for an insect to infest a new crop, and will compare the results from two different kinds of selection experiments. These publications will address fundamental questions in the literature on pest insects and their host relationships, including 1) What conditions are necessary for insects to shift to novel crop hosts? 2) Does genetic adaptation to a novel host necessarily lead to decreased performance on the ancestral host?, and 3)Do any of the genes modifying larval fitness in a new crop host also affect egg-laying behavior simultaneously, or are these important traits needed for colonization of a new host influenced by entirely different sets of genes? We hope
that our research results will address some long-standing questions regarding the nature of interactions between insect pests and their host plants.
Publications
- Messina, F.J., Morrey, J.L., and Mendenhall, M. 2007. Why do host-deprived seed beetles 'dump' their eggs?. Physiological Entomology 32:259-267.
- Messina, F.J., Bloxham, A.J., and Seargent, A.J. 2007. Mating compatibility between geographic populations of the seed beetle Callosobruchus maculatus. Journal of Insect Behavior 20:489-501.
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Progress 01/01/06 to 12/31/06
Outputs
We have continued to investigate processes that either promote or constrain the ability of seed beetles (Callosobruchus maculatus) to incorporate new crop hosts in their diets. We have been especially focused on beetle adaptation to lentil, Lens culinaris (= esculenta). A member of the tribe Viceae, lentil is a very poor host for C. maculatus, which typically attacks seeds in the tribe Phaseoleae, such as cowpea or mung bean. Infestation of stored lentils is rare even in regions where lentil is the dominant dietary legume, and beetle populations are generally unable to sustain positive growth on this host. An initial experiment demonstrated that larvae from a cowpea-adapted, African population and a mung bean-adapted, Asian population exhibited zero survival in lentils (out of 100 larvae). Nevertheless, we have successfully completed two mass-selection experiments that showed that the Asian population possessed rare alleles permitting good egg-to-adult survival in
lentil and positive population growth. In one experiment, survival rose from near zero percent to 75 percent in fewer than 10 generations. At the same time, there was a modest increase in the tendency of egg-laying females to accept lentil for oviposition. A hybridization experiment indicated that the mode of inheritance of the ability to survive in lentil is partially additive; analysis of F2 and backcross progeny will provide more specific information. In addition to the lentil-adaptation experiments, we continued an experiment in which replicate lines of an African popuation were shifted from their ancestral host, cowpea, to three other important grain legumes: mung bean, chickpea and adzuki bean. This experiment will compare the relative genetic lability of female egg-laying behavior vs. larval physiology. In particular, chickpea is a good larval host but elicits little oviposition, while females readily oviposit on adzuki beans, which confer low larval survival and slow
development. This experiment has now been maintained for more than 25 beetle generations, and we have assessed changes in beetle performance or behavior at several intervals.
Impacts
The seed beetle Callosobruchus maculatus is one of the most important pests of stored grain legumes or pulses in the world. It causes especially serious crop losses in developing countries of Asia and Africa, where storage facilities are inadequate, pesticides are costly, and, at the same time, grain legumes constitute an major source of protein. With the withdrawal of some commonly used insecticides for stored-product insects, control of these insects has become increasingly dependent on the development of resistant legumes varieties and species. Because insect populations are notorious for rapidly adapting to novel challenges in their environment (such as pesticides or previously resistant plants), it is important to isolate and identify the mechanisms by which insect populations are able to overcome plant-resistance traits. Our research examines the degree to which pest traits are modified as these insects adapt to novel crops. Understanding the processes by which
insects expand their host ranges will provide valuable information for other insect pests. We are especially interested in the relative importance of modification of larval vs. adult traits during the period of adaptation to new legume hosts.
Publications
- No publications reported this period
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Progress 01/01/05 to 12/31/05
Outputs
We continued to assess the genetic lability of morphological, physiological, and behavioral traits that permit seed beetles to attack new grain legume crops in storage. Replicate lines of an African population of Callosobruchus maculatus were shifted from their ancestral host, cowpea, to either mung bean (which confers slower development and smaller adult size), adzuki bean (a host that confers poor larval survival and very slow development), and chickpea (a host that is highly suitable to larvae but elicits little egg-laying by adult females). These hosts were chosen because they differ from cowpea in either their suitability for larval development or their attractiveness to egg-laying females. After 10 generations, we found little evidence of a shift in egg-laying behavior. In both choice and no-choice situations, lines transferred to the novel hosts exhibited preferences similar to those in lines maintained on the ancestral host. Larval performance did respond
rapidly to selection, however, as larvae from the lines transferred to adzuki beans displayed faster development and higher survival in this host than did lines maintained on cowpea. In addition to this selection experiment, which involved estimating the rate at which an African population adapted to moderately suitable hosts, we performed a second set of experiments to determine whether Asian or African beetle populations were able to adapt to two extremely poor hosts, lentil and soybean. At the start of the experiment, both hosts caused virtually 100% mortality of African or Asian larvae within seeds. In a mass-selection experiment, we transferred several thousand beetles from each of three replicate lines to soybean or lentil, and monitored whether beetle populations were able to sustain themselves in any of the host-line combinations. No population maintained itself on soybeans, but one of the Asian lines was found to slowly increase its densities in lentil cultures. After less
than 10 generations on lentil, this population exhibited >60% larval survival in the new host, whereas survival in the ancestral Asian population remained near zero. Future experiments will examine whether adapting to an extremely marginal host has altered beetle performance in the ancestral host. We will also compare the relative degree of modification of larval vs. adult traits in the lentil-adapted population. A final set of experiments compared how Asian and African beetle populations responded to host deprivation, i.e., an absence of host seeds. The two populations differed significantly in their responses; in the absence of seeds, African females tended to 'dump' their eggs on unsuitable substrates, whereas Asian beetles typically died without laying a single egg. Future experiments will attempt to explain why populations have diverged in this aspect of egg-laying behavior.
Impacts
The seed beetle Callosobruchus maculatus is a cosmopolitan pest of human stores of grain legumes. It causes particularly heavy crop losses in developing countries in Asia and Africa, where storage facilities are inadequate and, at the same time, grain legumes constitute an important source of protein. With the withdrawal of commonly used insecticides for stored-product insects, control of these insects has become increasingly dependent on the development of resistant legumes varieties and species. Because insect populations are notorious for rapidly adapting to novel challenges in their environment (such as pesticides or previously resistant plants), it is important to isolate and identify the mechanisms by which insect populations are able to overcome plant-resistance traits. Our research examines the degree to which larval and adult characteristics are modified as insects adapt to novel crops, which at the start of our experiments are sometimes much less suitable to
the beetle's familiar hosts. We are especially interested in the relative importance of modification of larval vs. adult traits during the period of adaptation to new legume hosts.
Publications
- Messina, F.J. 2004. Predictable modification of body size and competitive ability following a host shift by a seed beetle. Evolution 58: 2788-2797.
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Progress 01/01/04 to 12/31/04
Outputs
This project compares the genetic lability of traits that mediate shifts to novel grain-legume crops by a seed beetle pest, and attempts to determine whether there are genetic trade-offs associated with adaptation to a novel host. Initial experiments established baseline data on the performance of two geographic populations (African and Asian) of Callosobruchus maculatus on six economically important, grain-legume crops (cowpea, mung bean, adzuki bean, chickpea, lentil, and soybean). Measured fitness components included larval survival, larval development time, body mass at adult emergence, female egg-laying preferences, and total fecundity. These results were used to initiate a selection experiment using the African strain. Replicate lines from the African populations were either maintained on cowpea or switched to mung bean, adzuki bean (a host that confers low survival), or chickpea (a host that elicits little oviposition). Beetle performance will be assayed at
frequent intervals so as to determine the rate and trajectory of evolutionary change. An initial assay of female egg-laying preferences, conducted after five generations, indicated little or no change in female behavior in any of the lines transferred to the three novel hosts. Total fecundity and larval performance will be determined within ten generations from the start of the experiment. This replicated selection experiment will be augmented by a mass-selection experiment in which both the Asian and African populations will be used to measure adaptation to two extremely marginal hosts, soybean and lentil. Prior to selection, each of these hosts was found to elicit high levels of oviposition by C. maculatus females but more than 99% of larvae fail to survive to adult emergence.
Impacts
The research is examining genetic changes that accompany adaptation to novel hosts by a seed beetle, Callosobruchus maculatus. This beetle is a major stored-product pest in much of the world, especially where grain legumes constitute a major source of dietary protein. Limits to the host range of this pest are poorly understood; there are several anecdotal reports of isolated populations infesting atypical hosts (e.g., lentils, soybeans). Because control of these insects often relies on the development of resistant legume varieties, more information on the genetic basis of host use will help determine the feasibility and durability of varietal resistance. This information includes the rates and mechanisms by which beetles are able to overcome plant-resistance traits. We are examining the genetic lability of traits that determine adult egg-laying preferences as well as larval performance (survival, development time, body mass) within host seeds.
Publications
- Fox, C.W., Stillwell, R.C., Amarillo-S, A.R., Czesak, M.E.and Messina, F.J. 2004. Genetic architecture of population differences in oviposition behavior of the seed beetle Callosobruchus maculatus. J. Evol. Biol. 17:1141-1151.
- Messina, F.J. 2004. How labile are the egg-laying preferences of seed beetles? Ecological Entomology 29:318-326.
- Messina, F.J. and Bloxham, A.J.. 2004. Plant resistance to the Russian wheat aphid: effects of a nontarget aphid and the role of induction. The Canadian Entomologist 136:129-137.
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Progress 07/01/03 to 12/31/03
Outputs
This project aims to compare the genetic lability of traits that mediate shifts to novel crops by herbivorous insects, and to determine the presence and nature of trade-offs associated with adapting to a novel host. In the first phase of this project, we have established baseline data on the performance of the seed beetle Callosobruchus maculatus on six grain legume hosts (cowpea, mung bean, adzuki bean, chickpea, lentil, and soybean). Host acceptance, larval survival, larval development time, and adult body mass were measured on each host for two geographic populations: an African population adapted to cowpea and and Asian population adapted to mung bean. Analyses indicate a strong host effect as well as a host x population interaction, which suggests that the two populations respond differently to the six hosts. A quantitative-genetic experiment used a half-sib/full-sib split-brood design to measure standing genetic variation in the African population with respect
to performance on its usual host, cowpea, and a novel host mung bean (which is the familiar host of the Asian population). This experiment will be followed by selection experiments to compare the reliability of breeding designs vs. selection experiments in predicting adaptation to a novel host.
Impacts
The research will examine genetic changes that accompany adaptation to novel hosts by a seed beetle that is a major pest of stored grain legumes. Because control of these insects often relies on the development of resistant varieties, more information on the genetic basis of host use will help determine the feasibility and durability of varietal resistance. This information includes the rates and mechanisms by which beetles are able to overcome plant-resistance traits.
Publications
- Messina, F.J., and Karren, M.E. 2003. Adaptation to a novel host modifies host discrimination by the seed beetle, Callosobruchus maculatus. Animal Behaviour 65:501-507.
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