Genetics of oviposition-site preference in Drosophila tripunctata

Jaenike, John

doi:10.1038/hdy.1987.144

Cited by 56 publications

(42 citation statements)

References 16 publications

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“…Jaenike, 1987;Singer et al, 1992;Thompson, 1993), indicate that specialization in many phytophagous insects is evolutionarily dynamic rather than a dead end. This dynamic aspect of specialization creates the potential for strong geographic mosaics in patterns of specialization and in coevolution between insects and plants (Thompson, 1994a, b).…”

Section: Discussionmentioning

confidence: 99%

Trade‐offs in larval performance on normal and novel hosts

Thompson

1996

Entomologia Exp Applicata

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The evolution of host specialization in phytophagous insects is generally thought to involve genetic trade-offs that prevent individuals from maximizing fitness simultaneously on two or more hosts. Several hypotheses, however, have suggested that trade-offs may not be evident in experiments comparing larval performance on normal and novel hosts. Tests on survivorship, growth rate, and pupal mass among families of the swallowtail butterfly Papilio oregonius on its normal host and on a novel host provide support for these hypotheses, although they do not discriminate among them. Families differed in their relative performance on the hosts, but there was no evidence of a negative genetic correlation between hosts for any of the measures of performance. In addition, there were no correlations among the different measures, corroborating an earlier result suggesting that these different components of performance in the P machaon species group are under at least partially separate genetic control. These results and similar results published for other insects have now produced a body of studies indicating that genetic trade-offs in individual components of larval performance may not be a major factor preventing shifts onto novel host plants. Trade-offs leading to the evolution of host specialization are more likely to involve coordination among the various components of performance together with ecological factors that allow higher fitness on one host than on others.

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Section: Discussionmentioning

confidence: 99%

Trade‐offs in larval performance on normal and novel hosts

Thompson

1996

Entomologia Exp Applicata

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“…Theoretically, the quickest way to achieve speciation through host specialization is if host preference and performance each have a simple genetic architecture and are tightly linked to each other (Fry 2003). Jaenike (1987) posited that it is unlikely for linkage disequilibrium to establish a genetic correlation between preference and performance in a system with more than a few interacting alleles. More likely, pleiotropy would explain such a linkage.…”

Section: No Evidence For Genetic Linkage Between Preference and Tolermentioning

confidence: 99%

“…Early genetic data in Drosophila by Jaenike (1986Jaenike ( , 1987Jaenike ( , 1989 suggested that oviposition preference and "settling" behavior are unlinked in Drosophila tripunctata, while Taylor and Condra (1983) found linkage between preference and performance in D. pseudoobscura. No linkage was found in other herbivorous species, such as Callosobruchus maculatus (southern cowpea weevil; Wasserman and Futuyma 1981), Colias philodice (butterfly; Tabashnik 1986), Papilionidae (swallowtail butterflies; Thompson 1988;Thompson et al 1990), Chrysomelidae (leaf-feeding beetles; Keese 1996), Nilaparvata lugens (brown planthopper; Sezer and Butlin 1998a,b), and Oreina elongata (leaf beetle; Ballabeni and Rahier 2000).…”

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confidence: 99%

A Locus in Drosophila sechellia Affecting Tolerance of a Host Plant Toxin

et al. 2013

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Many insects feed on only one or a few types of host. These host specialists often evolve a preference for chemical cues emanating from their host and develop mechanisms for circumventing their host's defenses. Adaptations like these are central to evolutionary biology, yet our understanding of their genetics remains incomplete. Drosophila sechellia, an emerging model for the genetics of host specialization, is an island endemic that has adapted to chemical toxins present in the fruit of its host plant, Morinda citrifolia. Its sibling species, D. simulans, and many other Drosophila species do not tolerate these toxins and avoid the fruit. Earlier work found a region with a strong effect on tolerance to the major toxin, octanoic acid, on chromosome arm 3R. Using a novel assay, we narrowed this region to a small span near the centromere containing 18 genes, including three odorant binding proteins. It has been hypothesized that the evolution of host specialization is facilitated by genetic linkage between alleles contributing to host preference and alleles contributing to host usage, such as tolerance to secondary compounds. We tested this hypothesis by measuring the effect of this tolerance locus on host preference behavior. Our data were inconsistent with the linkage hypothesis, as flies bearing this tolerance region showed no increase in preference for media containing M. citrifolia toxins, which D. sechellia prefers. Thus, in contrast to some models for host preference, preference and tolerance are not tightly linked at this locus nor is increased tolerance per se sufficient to change preference. Our data are consistent with the previously proposed model that the evolution of D. sechellia as a M. citrifolia specialist occurred through a stepwise loss of aversion and gain of tolerance to M. citrifolia's toxins. HALF of all insects interact with plants (Grimaldi and Engel 2005). Most phytophageous insects, however, use only a few plant genera for food, mating, and oviposition (Bernays and Chapman 1994). Changes in host use can result in both new species and new adaptations (Ehrlich and Raven 1964;Janz 2011). For example, the evolution of a new host specialization may have contributed to the formation of new species in pea aphids (Acyrthosiphon) among others (Via 2001;Matsubayashi et al. 2010). Adapting to a new host can drive genetic and phenotypic change that is critical for isolating nascent species. In some cases, specialization has a price: Increased performance on the new host correlates with reduced performance on other hosts (Futuyma and Moreno 1988;Jaenike 1990;Fry et al. 1996;Scheirs et al. 2005; Via and Hawthorne 2005). This scenario poses a new challenge for the nascent specialist, as it must keep together alleles for finding and selecting the appropriate host ("preference") along with those for utilizing that host ("performance," e.g., physiologically adapting to that host's secondary compounds or nutritional content; Jaenike 1990; Janz 2011). Theory suggests that a genetic correlation betwe...

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“…Specialists often evolve host-specific adaptations such as resistance to plant secondary compounds, changes in morphology, and new preference behaviors. An understanding of the genetic basis of traits such as these is critical to knowing how host specialization evolves ( Jaenike 1987;Via 1990;Futuyma 1991;Jaenike and Holt 1991;Hawthorne and Via 2001).…”

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confidence: 99%

Genetic Changes Accompanying the Evolution of Host Specialization in Drosophila sechellia

2009

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Changes in host specialization contribute to the diversification of phytophagous insects. When shifting to a new host, insects evolve new physiological, morphological, and behavioral adaptations. Our understanding of the genetic changes responsible for these adaptations is limited. For instance, we do not know how often host shifts involve gain-of-function vs. loss-of-function alleles. Recent work suggests that some genes involved in odor recognition are lost in specialists. Here we show that genes involved in detoxification and metabolism, as well as those affecting olfaction, have reduced gene expression in Drosophila sechellia-a specialist on the fruit of Morinda citrifolia. We screened for genes that differ in expression between D. sechellia and its generalist sister species, D. simulans. We also screened for genes that are differentially expressed in D. sechellia when these flies chose their preferred host vs. when they were forced onto other food. D. sechellia increases expression of genes involved with oogenesis and fatty acid metabolism when on its host. The majority of differentially expressed genes, however, appear downregulated in D. sechellia. For several functionally related genes, this decrease in expression is associated with apparent loss-of-function alleles. For example, the D. sechellia allele of Odorant binding protein 56e (Obp56e) harbors a premature stop codon. We show that knockdown of Obp56e activity significantly reduces the avoidance response of D. melanogaster toward M. citrifolia. We argue that apparent loss-of-function alleles like Obp56e potentially contributed to the initial adaptation of D. sechellia to its host. Our results suggest that a subset of genes reduce or lose function as a consequence of host specialization, which may explain why, in general, specialist insects tend to shift to chemically similar hosts.

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Genetics of oviposition-site preference in Drosophila tripunctata

Cited by 56 publications

References 16 publications

Trade‐offs in larval performance on normal and novel hosts

Trade‐offs in larval performance on normal and novel hosts

A Locus in Drosophila sechellia Affecting Tolerance of a Host Plant Toxin

Genetic Changes Accompanying the Evolution of Host Specialization in Drosophila sechellia

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