Evolution of mito-nuclear interactions: „mother’s curse“ and the „Trojan Female Technique“ for biocontrol of seed beetle (Acanthoscelides obtectus, Say) populations

[L. Vlajnić]

137 str.

Biologija - Evoluciona biologija / Biology - Evolutionary biology

Evoluciona teorija predviđa da su mitohondrijski genomi skloni nakupljanju mutacija sa negativnim efektom za mužjake, a neutralnim ili pozitivnim za ženke, što predstavlja fenomen materinske kletve. Ovakve mutacije, ukoliko imaju negativan efekat na reproduktivni potencijal mužjaka, mogu biti iskorišćene u novopredloženoj metodi kontrole ekonomski štetnih vrsta insekata, tehnici trojanskih ženki (TTŽ). Ova metoda zasniva se na ubacivanju ženki nosilaca opisane mitohondrijske mutacije, trojanskih ženki, u prirodne populacije. Žensko potomstvo ovih ženki biće fertilno i prenosiće mutaciju niz generacije, dok će muško biti sterilno, što će za rezultat imati pad brojnosti populacije kroz generacije. Ipak, imajući u vidu da mitohondrijski i jedarni genom interaguju i koevoluiraju, selekcija će favorizovazi jedarne kompenzacione mutacije koje maskiraju negativan efekat mitohondrijskih mutacija na mužjake. Vodeći se ovim teorijskim postavkama, u laboratorijskim populacijama pasuljevog žiška (Acanthoscelides obtectus) utvrđeno je postojanje efekta materinske kletve, tj. veće varijanse u osobinama životne istorije kod mužjaka različitih mitohondrijskih genotipova (mitotipova) u odnosu na ženke. Konkretno, identifikovan je i genetički okarakterisan specifičan MG3b mitotip koji dovodi do smanjenja ranog fekunditeta i fertiliteta mužjaka, a nema efekat na iste osobine kod ženki. Zbog svog uticaja na fertilitet mužjaka, MG3b mitotip označen je kao kandidat za primenu u TTŽ-u. Kod mužjaka ovog mitotipa, u odnosu na kontrolne mitotipove, demonstriran je pad respiratorne funkcije svih kompleksa mitohondrijskog sistema oksidativne fosforilacije (OXPHOS). Ovaj pad je najverovatniji uzrok smanjenja reproduktivne funkcije MG3b mužjaka budući da su spermatozoidi i muško germinativno tkivo posebno osetljivi na promene u aktivnosti OXPHOS. Pokazano je i da MG3b mitotip dovodi do pada fertiliteta mužjaka u jedarnim sredinama poreklom iz različitih prirodnih populacija i da ovaj efekat ne zavisi od mito-jedarnih interakcija. Međutim, na povišenu temperaturu MG3b mužjaci reaguju povećanjem fertiliteta, što ukazuje na potencijalni fenomen mitohormeze. Nakon ubacivanja trojanskih ženki MG3b mitotipa u prirodnu populaciju nije utvrđen pad brojnosti populacije kroz generacije. Populaciono-genetička analiza pokazala je da su populacije pasuljevog žiška slabo strukturirane što ih čini pogodnim za dalju potragu za mutacijama materinske kletve. Rezultati ove disertacije potvrdili su fenomen materinske kletve u populacijama pasuljevog žiška i upućuju na to da bi, uz podrobnija istraživanja, pronađene mutacije sa negativnim efektom na fertilitet mužjaka mogle da se koriste u TTŽ-u.

The evolutionary theory posits that mitochondrial genomes are susceptible to accumulating mutations that can have detrimental effects on males, while being neutral or even beneficial for females. This phenomenon is known as the mother’s curse. Mutations that negatively impact male reproductive potential could be used in a newly proposed method for controlling economically damaging insect species, referred to as the Trojan Female Technique. This approach involves introducing females carrying the specified mitochondrial mutation, termed Trojan females, into natural populations. The female offspring of these Trojan females will be fertile and will transmit the mutation through subsequent generations, while their male offspring will be sterile, resulting in a gradual decline in population numbers over time. However, given the interaction and co-evolution of mitochondrial and nuclear genomes, nuclear compensatory mutations that mitigate the effects of mitochondrial mutations on males would likely be favored. Based on these theoretical foundations, the impact of the mother’s curse has been demonstrated in laboratory populations of the seed beetle (Acanthoscelides obtectus), revealing greater variance in life history traits among males with different mitochondrial genotypes (mitotypes) compared to females. Notably, a specific MG3b mitotype has been identified, which reduces early fecundity and fertility in males without affecting these traits in females. This mitotype has been genetically characterized and marked as a candidate for application in the Trojan Female Technique. In males with the MG3b mitotype, a decline in respiratory function across all complexes of mitochondrial oxidative phosphorylation (OXPHOS) has been observed, likely contributing to the reduction in reproductive function, as spermatozoa and male germinative tissue are particularly sensitive to changes in the oxidative phosphorylation system's activity. Furthermore, it has been established that the MG3b mitotype leads to decreased male fertility in nuclear environments derived from various natural populations, and this effect is independent of mito-nuclear interactions. Interestingly, at elevated temperatures, MG3b males exhibit increased fertility, suggesting a potential phenomenon of mitohormesis. After the introduction of Trojan females carrying the MG3b mitotype into the natural population, no decline in population numbers across generations was noted. Population-genetic analysis indicated that seed beetle populations are poorly structured, making them ideal for further exploration of mother’s curse mutations. The findings of this dissertation confirm the existence of the mother’s curse in seed beetle populations and suggest that with more comprehensive research, the identified mutations affecting male fertility could be effectively utilized in the Trojan Female Technique.

mitohondrije, mitotip, materinska kletva, tehnika trojanskih ženki, mito-jedarne interakcije, reproduktivni potencijal, mitohondrijska funkcija, Acanthoscelides obtectus

mitochondria, mitotype, mother’s curse, Trojan Female Technique, mito-nuclear interactions, reproductive potential, mitochondrial function, Acanthoscelides obtectus

575.827:576.311.347:575.113.3:57.017.5]:595.768.1(043.3)

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