Decoding the Olive Fly's Symbiotic Secret

The olive fruit fly (Bactrocera oleae) is the most sig­nif­i­cant olive grove pest in the Mediterranean region and world­wide.

The dam­age is caused by its lar­vae, which feed on the olive fruit, caus­ing sig­nif­i­cant quan­ti­ta­tive and qual­i­ta­tive losses in fruit and oil.

Each year, the pest accounts for more than 30 per­cent of the destruc­tion of all Mediterranean olive crops, which equates to annual losses of almost €3 bil­lion.

Insecticides have long been the pri­mary recourse against olive fruit fly infes­ta­tion, as in the case of many other olive pests, such as the olive moth.

Environmental impacts, such as tox­i­c­ity to non-tar­get organ­isms, aquatic pol­lu­tion and human food chain con­t­a­m­i­na­tion, have resulted in the recent with­drawal of an unprece­dented num­ber of insec­ti­cide com­po­nents via the imple­men­ta­tion of European Union reg­u­la­tions.

In addi­tion, the wide­spread use of pes­ti­cides com­bined with the pest organ­isms’ brief life cycles has resulted in resis­tant strains.

Unlike most other pests, how­ever, the olive fruit fly almost entirely relies upon a sym­bi­otic bac­terium, namely Candidatus Erwinia daci­cola.

The insect lar­vae require this sym­biont to feed upon imma­ture green olives by over­com­ing the olive’s nat­ural chem­i­cal defenses, such as oleu­ropein, and is an impor­tant fac­tor in lar­val devel­op­ment when feed­ing upon black olives.

It also increases egg pro­duc­tion in adult females under stress­ful con­di­tions.

Because of this unique rela­tion­ship between insect and bac­terium, Ca. E. daci­cola has been the sub­ject of recent research into novel con­trol meth­ods.

It has been shown, for exam­ple, that cer­tain antimi­cro­bial com­pounds, such as cop­per oxy­chlo­ride and virid­iol, can inter­fere with the sym­bi­otic rela­tion­ship, lead­ing to dis­rupted lar­val devel­op­ment and decreased har­di­ness in adults.

New research pub­lished in Nature seeks to pro­vide a more com­pre­hen­sive knowl­edge base on which to build by car­ry­ing out the most detailed genetic study into the olive fruit fly and its sym­biont.

The study exam­ined both organ­isms’ bio-geo­graphic pat­terns and genetic diver­sity across 54 pop­u­la­tions span­ning the Mediterranean, Africa, Asia and the Americas.

The researchers iden­ti­fied three pri­mary bac­te­r­ial hap­lo­types: htA, htB and htP.

Haplotypes htA and htB dom­i­nated the Mediterranean region, with htA preva­lent in west­ern pop­u­la­tions (e.g., Algeria, Morocco and the Iberian penin­sula) and htB in east­ern areas (e.g., Israel, Turkey and Cyprus).

Central Mediterranean pop­u­la­tions exhib­ited a mix­ture of these hap­lo­types, reflect­ing a con­flu­ence zone influ­enced by the migra­tion and selec­tion of olive cul­ti­vars.

Archaeological evi­dence sug­gests that olives were domes­ti­cated in the east­ern Mediterranean and spread west­ward. The researchers note that the genetic pat­terns of the olive fly and its sym­biont align with these move­ments, indi­cat­ing that human selec­tion of olive cul­ti­vars likely influ­enced the dis­tri­b­u­tion and adap­ta­tion of the pest and its sym­biont.

For exam­ple, the genetic admix­ture of the cen­tral Mediterranean pop­u­la­tions is con­sis­tent with the blend­ing of east­ern and west­ern olive lin­eages.

Haplotype htP, unique to Pakistan, like­wise high­lights ancient geo­graphic sep­a­ra­tion and evo­lu­tion­ary diver­gence, with the symbiont’s lower genetic diver­sity than the host fly sug­gest­ing a long-term asso­ci­a­tion char­ac­ter­ized by selec­tive pres­sures.

South African pop­u­la­tions were sim­i­larly dis­tinct, reflect­ing the fly’s and its host’s evo­lu­tion­ary his­tory.

Other geo­graph­i­cally iso­lated pop­u­la­tions, such as those found in Crete, California and Iran, were par­tic­u­larly use­ful in mod­el­ing dis­per­sal and adap­ta­tion pat­terns.

Crete, for exam­ple, har­bors pre­dom­i­nantly htA despite its prox­im­ity to east­ern regions, likely due to his­tor­i­cal iso­la­tion and lim­ited gene flow.

Californian pop­u­la­tions share east­ern Mediterranean sym­biont and host hap­lo­types, sup­port­ing the hypoth­e­sis of human-medi­ated intro­duc­tion from Turkey.

Similarly, Iranian pop­u­la­tions show strong genetic ties to cen­tral Mediterranean pop­u­la­tions, sug­gest­ing recent intro­duc­tions and spread within the region.

The researchers believe that this deeper under­stand­ing of the genetic struc­ture of olive fly pop­u­la­tions and their sym­bionts can inform tar­geted inter­ven­tions.

For instance, the dis­tinct genetic pro­files of Pakistani and South African pop­u­la­tions may neces­si­tate region-spe­cific approaches.

The study also under­scored the poten­tial for lever­ag­ing sym­biont biol­ogy in pest man­age­ment, such as by dis­rupt­ing the bacterium’s role in over­com­ing olive defenses.

• Insect Biochemistry and Molecular Biology