Award Abstract # 1557697
Genetic Analysis and Life History Consequences of Variation in Larval Behavior in Cactophilic Drosophila

NSF Org: IOS
Division Of Integrative Organismal Systems
Recipient: THE UNIVERSITY OF ALABAMA IN HUNTSVILLE
Initial Amendment Date: May 25, 2016
Latest Amendment Date: April 12, 2017
Award Number: 1557697
Award Instrument: Standard Grant
Program Manager: Patrick Abbot
dabbot@nsf.gov
 (703)292-0000
IOS
 Division Of Integrative Organismal Systems
BIO
 Directorate for Biological Sciences
Start Date: June 1, 2016
End Date: May 31, 2021 (Estimated)
Total Intended Award Amount: $612,000.00
Total Awarded Amount to Date: $612,000.00
Funds Obligated to Date: FY 2016 = $612,000.00
History of Investigator:
  • Luis Cruz-Vera (Principal Investigator)
    lrc0002@uah.edu
  • Luciano Matzkin (Former Principal Investigator)
Recipient Sponsored Research Office: University of Alabama in Huntsville
301 SPARKMAN DR NW
HUNTSVILLE
AL  US  35805-1911
(256)824-2657
Sponsor Congressional District: 05
Primary Place of Performance: University of Alabama in Huntsville
301 Sparkman Drive
Huntsville
AL  US  35805-1911
Primary Place of Performance
Congressional District:
05
Unique Entity Identifier (UEI): HB6KNGVNJRU1
Parent UEI:
NSF Program(s): Animal Behavior,
EPSCoR Co-Funding
Primary Program Source: 01001617DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 1228, 9150, 9178, 9179
Program Element Code(s): 765900, 915000
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.074

ABSTRACT

Some of the most fundamental questions in biology pertain to understanding speciation. A strong driving force in speciation is adaptation to the local environment a population resides in, which can lead to splitting gene pools apart. If two populations of the same species living in distinct environments are adapted to their local ecological conditions, offspring between the two populations may not survive as well and ultimately reduce the exchange of genetic information between populations. It is the formation of this genetic isolation that can lead populations to become different species. This study focuses on two populations of a cactus-breeding fly, Drosophila mojavensis, which live in different environments, use different cactus species, and have distinct larval behaviors. In one population the larvae feed on small cactus pads (prickly pear) and don't move much, while the other population feeds on larger cactus (organpipe) and move more and faster. Capitalizing on the rich genetic 'toolkit' for Drosophila this study will identify the genes responsible for these differences and determine how changes at the gene level can lead to different behaviors and population isolation. Information from this research will be shared with the science community through publications and presentations. The investigator will mentor students through research in behavioral genetics and will use the funded techniques in research-focused college courses. Also the investigator will partner with local high schools to expose students to research at the university level.

Understanding the evolution and underlying genetics of alternative larval behaviors could be instrumental in elucidating how adaptation to local ecological conditions can lead to the divergence of populations, speciation, and how genotypes lead to behavioral phenotypes. Ecological adaptation has a significant influence on the variation seen in behavioral strategies. In saprophytic and phytophagous insects the properties of the plant host have been shown to greatly influence the pattern of genomic, metabolomics, physiological, life history and behavioral variation. It is this divergent, ecologically-driven adaptation to a host's properties that can drive the evolution of reproductive incompatibilities between host populations and lead to the formation of species. This study will focus on the variation of larval activity, and its underlying genetic control, of the cactophilic Drosophila mojavensis. Distinct populations of D. mojavensis have nutritionally and chemically distinct cactus hosts, which are associated with different larval behaviors. The study will examine the physiology and life history consequence of the distinct behaviors and link it to the transcriptional and genomic changes between the distinct cactus host populations of D. mojavensis. A quantitative trait loci analysis will examine the genetic underpinnings of larval behavior. CRISPR-Cas9 knockouts and transgenics will be generated to quantify the functional role of the candidate behavior QTLs in an ecological context and examine the life history consequences of variation at these loci and provide a strong examination of genotype to phenotype level questions.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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Carson W. Allan and Luciano M. Matzkin "Genomic analysis of the four ecologically distinct cactus host populations of Drosophila mojavensis" BMC Genomics , v.20 , 2019 , p.732 10.1186/s12864-019-6097-z.
Coline C. JaworskiCarson W. AllanLuciano M. Matzkin "Chromosome-level hybrid de novo genome assemblies as an attainable option for non-model insects." Molecular Ecology Resources , 2020 10.1111/1755-0998.13176
Fernando DiazBram KuijperRebecca B. HoyleJoshua M. ColemanNathaniel TalamantesLuciano M. Matzkin "Environmental predictability drives adaptive within- and transgenerational plasticity of heat tolerance across life stages and climatic regions." Functional Ecology , v.35 , 2021 , p.153 10.1111/1365-2435.13704
Fernando Diaz, Carson W. Allan, and Luciano M. Matzkin "Positive selection drives the evolution of cactophilic Drosophila chemosensory genes following a recent divergence shaped by multiple host shifts" BMC Evolutionary Biology , v.18 , 2018 10.1186/s12862-018-1250-x
Joshua M. Coleman, Kyle M. Benowitz, Alexandra G. Jost, Luciano M. Matzkin "Behavioral evolution accompanying host shifts in cactophilic Drosophila larvae" Ecology and Evolution , v.24 , 2018 DOI: 10.1002/ece3.4209
Khallaf, M.A., Auer, T.O., Grabe, V., Depetris-Chauvin, A. Ammagarahalli, B., Zhang, D., Lavista-Llanos, S., Kaftan, F., Weibflog, J., Matzkin L. M., Rollmann, S.M., Lofstedt, C., Svatos, A., Dweck, H.K.M., Sachse, S., Benton, R., Hansson, B.S., and Knade "A male pheromone promotes incipient isolation through conserved peripheral sensory pathways." Science Advances , v.6 , 2020 10.1126/sciadv.aba5279
Kyle M. Benowitz, Joshua M. Coleman and Luciano M. Matzkin "Assessing the Architecture of Drosophila mojavensis Locomotor Evolution with Bulk Segregant Analysis" G3 , v.9 , 2019 , p.1767 10.1534/g3.119.400036
Kyle M. BenowitzJoshua M ColemanCarson W. AllanLuciano M. Matzkin "Gene expression in the Drosophila mojavensis brain reveals tissue specific cis-regulatory and compensatory evolution across populations." Genome Biology and Evolution , 2020 10.1093/gbe/evaa145

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

As we look at the natural world around us, we are exposed to organisms in their natural habitats.  Be it under the forest leaf litter, in a shallow stream, a rocky desert mountain, on a savannah, or any other habitat on Earth, we can often identify traits that organisms have that provide advantages or adaptation to the environments in which they live.  These traits are often the results of natural selection, shaping them over thousand or millions of generations.  Of note, is the fact that the work of natural selection is ecologically-context dependent; therefore, local ecological conditions can reshape and reorient the evolutionary trajectory of traits, and hence species.  This fundamental question is central to all the specific aims of this proposal. 

To provide further understanding on the genetics of traits associated with local ecological adaptation, we focused our work on a species of small desert-dwelling flies (Drosophila mojavensis).  These flies lay their eggs, develop, and feed as adults in the necrotic tissues of cacti, hence referred to as cactophilic Drosophila.  This particular species resides in the deserts of southern California, Arizona, and northwest Mexico, and is composed of four ecologically distinct populations.  Here we focused on two, a population from the Sonoran desert which utilizes necrotic organ pipe cactus (Stenocereus thurberi) and one from Santa Catalina Island (California) that utilizes necrotic prickly pear (Opuntia littoralis).  Our previous studies and that of others have shown that these populations have distinct adaptations and behaviors associated with the distinct cacti they use.  Among these adaptations is the behavior of larvae eating the rotten cactus, as well as how well they can withstand desiccation (lack of water), how quickly they developed from egg to adult and the shape and size of their wings.  We hypothesize that the fact that Catalina Island individuals live in small prickly pear pads rots that are common but usable for them for about a week or two versus Sonoran individuals living on large organ pipe rots that are relatively rare but can last months had distinctly shaped the behavior, morphology and physiology of these populations. 

We took a genomic approach to reveal the genes associated with some of these traits to understand the process of adaptation to local ecological conditions.  We first sequenced the genome of both populations to have a good reference of the distinct genomic differences between them.  We mixed the populations (i.e. mix their genomes) in the lab for about 40 generations and then measured a number of behavioral and morphological traits in individual flies and sequenced the entire genome of each individual fly, a total of over 2,000 genomes.  We then essentially asked which allele (Sonora vs. Catalina Island) is associated with a trait (e.g. fast larval speed), so we can link genes to specific traits.  By doing this we were able to uncover the genetic structure of a number of ecologically important traits.  This allowed us to not only understand how local ecological conditions shaped the evolution of these traits, but this information can also be used more broadly try to predict how populations can respond to future ecological changes.


Last Modified: 10/04/2021
Modified by: Luis R Cruz-Vera

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