Parasites Mediate Condition-Dependent Sexual Selection for Local Adaptation in a Natural Insect Population

Gómez‐Llano, Miguel; Narasimhan, Aaditya; Svensson, Erik I.

doi:10.1101/563874

Cited by 3 publications

(4 citation statements)

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“…shared mites [ 100 ] or parasitoids [ 101 ]). Damselflies are well-known for carrying and sharing ectoparasitic water mites [ 41 , 102 ], however the role of such parasites as vectors of Wolbachia among Ischnura species remains unknown. In contrast, evidences of frequent hybridization and introgression have been shown in some odonate species due to latitudinal range expansion and the increasing sympatric interactions between closely related species [ 103 ], including in the genus Ischnura [ 34 – 36 , 104 ].…”

Section: Discussionmentioning

confidence: 99%

Wolbachia-driven selective sweep in a range expanding insect species

et al. 2021

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Background Evolutionary processes can cause strong spatial genetic signatures, such as local loss of genetic diversity, or conflicting histories from mitochondrial versus nuclear markers. Investigating these genetic patterns is important, as they may reveal obscured processes and players. The maternally inherited bacterium Wolbachia is among the most widespread symbionts in insects. Wolbachia typically spreads within host species by conferring direct fitness benefits, and/or by manipulating its host reproduction to favour infected over uninfected females. Under sufficient selective advantage, the mitochondrial haplotype associated with the favoured maternally-inherited symbiotic strains will spread (i.e. hitchhike), resulting in low mitochondrial genetic variation across the host species range. Method The common bluetail damselfly (Ischnura elegans: van der Linden, 1820) has recently emerged as a model organism for genetics and genomic signatures of range expansion during climate change. Although there is accumulating data on the consequences of such expansion on the genetics of I. elegans, no study has screened for Wolbachia in the damselfly genus Ischnura. Here, we present the biogeographic variation in Wolbachia prevalence and penetrance across Europe and Japan (including samples from 17 populations), and from close relatives in the Mediterranean area (i.e. I. genei: Rambur, 1842; and I. saharensis: Aguesse, 1958). Results Our data reveal (a) multiple Wolbachia-strains, (b) potential transfer of the symbiont through hybridization, (c) higher infection rates at higher latitudes, and (d) reduced mitochondrial diversity in the north-west populations, indicative of hitchhiking associated with the selective sweep of the most common strain. We found low mitochondrial haplotype diversity in the Wolbachia-infected north-western European populations (Sweden, Scotland, the Netherlands, Belgium, France and Italy) of I. elegans, and, conversely, higher mitochondrial diversity in populations with low penetrance of Wolbachia (Ukraine, Greece, Montenegro and Cyprus). The timing of the selective sweep associated with infected lineages was estimated between 20,000 and 44,000 years before present, which is consistent with the end of the last glacial period about 20,000 years. Conclusions Our findings provide an example of how endosymbiont infections can shape spatial variation in their host evolutionary genetics during postglacial expansion. These results also challenge population genetic studies that do not consider the prevalence of symbionts in many insects, which we show can impact geographic patterns of mitochondrial genetic diversity.

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Section: Discussionmentioning

confidence: 99%

Wolbachia-driven selective sweep in a range expanding insect species

et al. 2021

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“…shared mites [76], or shared parasitoids [77]). Damsel ies are well-known for carrying and sharing ectoparasitic water mites [38,78], however the role of such parasites as vectors of Wolbachia between Ischnura species remains unknown. Additionally, the presence of wEle1 in both I. elegans and I. genei may rather suggest that horizontal transfer of the strain between the two species occurred through hybridization, as both species carry the same mitochondrial haplotype.…”

Section: Discussionmentioning

confidence: 99%

Wolbachia-driven selective sweep in a range expanding insect species

Deng

Assandri

Chauhan

et al. 2021

Preprint

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BackgroundEvolutionary processes can cause strong spatial genetic signatures, such as local loss of genetic diversity, or conflicting histories from mitochondrial versus nuclear markers. Investigating these genetic patterns is important, as they may reveal obscured processes and players. The maternally inherited bacterium Wolbachia is among the most widespread symbionts in insects. Wolbachia typically spreads within host species by conferring direct fitness benefits, or by manipulating its host reproduction to favour infected over uninfected females. Under sufficient selective advantage, the mitochondrial haplotype associated with the favoured symbiotic strains will spread (i.e. hitchhike), resulting in low mitochondrial genetic variation across the host species range. The common bluetail damselfly (Ischnura elegans: van der Linden, 1820) has recently emerged as a model organism of the genetics and genomic signatures of range expansion during climate change. Although there is accumulating data on the consequences of such expansion on the genetic of I. elegans, no study has screened for Wolbachia in the damselfly genus Ischnura. Here, we present the biogeographic variation in Wolbachia prevalence and penetrance in 17 I. elegans populations across Europe and Japan, and from close relatives in the Mediterranean area (i.e. I. genei: Rambur, 1842; and I. saharensis: Aguesse, 1958). ResultsOur data reveal (a) multiple Wolbachia-strains, (b) potential transfer of the symbiont through hybridization, (c) higher infection rates at higher latitudes, and (d) reduced mitochondrial diversity in the north-west populations, indicative of hitchhiking associated with the selective sweep of the most common strain. We found low mitochondrial haplotype diversity in the Wolbachia-infected north-western European populations (Sweden, Scotland, the Netherlands, Belgium, France and Italy) of I. elegans, and, conversely, higher mitochondrial diversity in populations with low penetrance of Wolbachia (Ukraine, Greece, Montenegro and Cyprus). The timing of the selective sweep associated with infected lineages was estimated between 20 000 to 44 000 years before present, which is consistent with the end of the last glacial period about 20 000 ya. ConclusionsOur findings provide an example of how endosymbiont infections ca shape spatial variation in their host evolutionary genetics during postglacial expansion. These results also challenge population genetic studies that do not consider the prevalence of symbionts in many insects, which can impact geographic patterns of mitochondrial genetic diversity.

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“…While it is easy to agree with the general gist of the statement, and generally expect that sexual or social traits can evolve to exploit conspecifics even if they are detrimental to group or population fitness [55][56][57][58], the question of the net effect is ultimately an empirical one. In bovids, large horns appear to increase extinction risk [59], and for sexual selection as a whole, the jury is still out [42,[59][60][61][62][63][64][65]. A mix of results, from negative to positive, is not wholly unexpected in a situation where theory shows sexual selection to have the potential to elevate female fitness.…”

Section: It Is Not All About Food: Individual Success At the Expense Of Conspecificsmentioning

confidence: 99%

“…There are numerous examinations of how sexual selection and sexual conflict relate to growth or stability, resilience against extinction via inbreeding, or other proxies of population fitness (review: [69], newer work: [59][60][61][62][63][64][65][70][71][72][73][74]). To make sense of the diverse mess, systematic approaches appear welcome.…”

Section: It Is Not All About Food: Individual Success At the Expense Of Conspecificsmentioning

confidence: 99%

The stagnation paradox: the ever-improving but (more or less) stationary population fitness

Kokko

2021

Proc. R. Soc. B.

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Fisher's fundamental theorem states that natural selection improves mean fitness. Fitness, in turn, is often equated with population growth. This leads to an absurd prediction that life evolves to ever-faster growth rates, yet no one seriously claims generally slower population growth rates in the Triassic compared with the present day. I review here, using non-technical language, how fitness can improve yet stay constant (stagnation paradox), and why an unambiguous measure of population fitness does not exist. Subfields use different terminology for aspects of the paradox, referring to stasis, cryptic evolution or the difficulty of choosing an appropriate fitness measure; known resolutions likewise use diverse terms from environmental feedback to density dependence and ‘evolutionary environmental deterioration’. The paradox vanishes when these concepts are understood, and adaptation can lead to declining reproductive output of a population when individuals can improve their fitness by exploiting conspecifics. This is particularly readily observable when males participate in a zero-sum game over paternity and population output depends more strongly on female than male fitness. Even so, the jury is still out regarding the effect of sexual conflict on population fitness. Finally, life-history theory and genetic studies of microevolutionary change could pay more attention to each other.

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Parasites Mediate Condition-Dependent Sexual Selection for Local Adaptation in a Natural Insect Population

Cited by 3 publications

References 70 publications

Wolbachia-driven selective sweep in a range expanding insect species

Wolbachia-driven selective sweep in a range expanding insect species

Wolbachia-driven selective sweep in a range expanding insect species

The stagnation paradox: the ever-improving but (more or less) stationary population fitness

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Parasites Mediate Condition-Dependent Sexual Selection for Local Adaptation in a Natural Insect Population

Cited by 3 publications

References 70 publications

Wolbachia-driven selective sweep in a range expanding insect species

Wolbachia-driven selective sweep in a range expanding insect species

Wolbachia-driven selective&nbsp;sweep&nbsp;in a range expanding&nbsp;insect&nbsp;species

The stagnation paradox: the ever-improving but (more or less) stationary population fitness

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Wolbachia-driven selective sweep in a range expanding insect species