Sexual selection expedites the evolution of pesticide resistance

Jacomb, Frances; Marsh, Jason N.; Holman, Luke

doi:10.1111/evo.13074

Cited by 27 publications

(29 citation statements)

References 44 publications

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“…The results from females assayed with enforced monogamy suggest that sexual selection is acting to enhance the promotion of beneficial alleles within a population and facilitate adaptation to increasing temperatures through 'good genes' mechanisms of sexual selection. This indicates that when the environment changes continuously, sexual selection can provide similar benefits to those found by previous empirical studies which examined the effect of sexual selection on adaptation when the environment undergoes a step change [25][26][27]. In this case, however, the improved fitness associated with strong sexual selection was not sufficient to delay extinction as temperatures continuously increased.…”

Section: Discussionsupporting

confidence: 64%

The effect of sexual selection on adaptation and extinction under increasing temperatures

Parrett¹,

Knell²

2018

Proc. R. Soc. B.

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Strong sexual selection has been reported to both enhance and hinder the adaptive capacity and persistence of populations when exposed to novel environments. Consequently, how sexual selection influences population adaption and persistence under stress remains widely debated. Here, we present two empirical investigations of the fitness consequences of sexual selection on populations of the Indian meal moth, exposed to stable or gradually increasing temperatures. When faced with increasing temperatures, strong sexual selection was associated with both increased fecundity and offspring survival compared with populations experiencing weak sexual selection, suggesting sexual selection acts to drive adaptive evolution by favouring beneficial alleles. Strong sexual selection did not, however, delay extinction when the temperature became excessively high. By manipulating individuals' mating opportunities during fitness assays, we were able to assess the effect of multiple mating independently from the effect of population-level sexual selection, and found that polyandry has a positive effect on both fecundity and offspring survival under increasing temperatures in those populations evolving with weak sexual selection. Within stable temperatures, there were some benefits from strong sexual selection but these were not consistent across the entire experiment, possibly reflecting changing costs and benefits of sexual selection under stabilizing and directional selection. These results indicate that sexual selection can provide a buffer against climate change and increase adaptation rates within a continuously changing environment. These positive effects of sexual selection may, however, be too small to protect populations and delay extinction when environmental changes are relatively rapid.

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Section: Discussionsupporting

confidence: 64%

The effect of sexual selection on adaptation and extinction under increasing temperatures

Parrett¹,

Knell²

2018

Proc. R. Soc. B.

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“…Evidence that sexual selection helps to fix beneficial alleles more effectively when environments change also varies, with some studies reporting that sexual selection improves adaptation to a novel environment (Fricke and Arnqvist ), aids the evolution of pesticide resistance (Jacomb et al. ), or prevents extinction (Plesnar‐Bielak et al. ).…”

Section: Discussionmentioning

confidence: 99%

“…In a mutation accumulation study with D. serrata, sexual selection did not prevent fitness reductions associated with the buildup of load, but did strengthen the fitness correlation between males and females, indicating an importance for sex-limited genetic load for population fitness (Allen et al 2017). Evidence that sexual selection helps to fix beneficial alleles more effectively when environments change also varies, with some studies reporting that sexual selection improves adaptation to a novel environment (Fricke and Arnqvist 2007), aids the evolution of pesticide resistance (Jacomb et al 2016), or prevents extinction (Plesnar-Bielak et al 2012). However, others have found no equivalent benefit (Holland 2002;Rundle et al 2006) or even antagonism against adaptation (Chenoweth et al 2015).…”

Section: Discussionmentioning

confidence: 99%

Lineages evolved under stronger sexual selection show superior ability to invade conspecific competitor populations

et al. 2018

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Despite limitations on offspring production, almost all multicellular species use sex to reproduce. Sex gives rise to sexual selection, a widespread force operating through competition and choice within reproduction, however, it remains unclear whether sexual selection is beneficial for total lineage fitness, or if it acts as a constraint. Sexual selection could be a positive force because of selection on improved individual condition and purging of mutation load, summing into lineages with superior fitness. On the other hand, sexual selection could negate potential net fitness through the actions of sexual conflict, or because of tensions between investment in sexually selected and naturally selected traits. Here, we explore these ideas using a multigenerational invasion challenge to measure consequences of sexual selection for the overall net fitness of a lineage. After applying experimental evolution under strong versus weak regimes of sexual selection for 77 generations with the flour beetle Tribolium castaneum, we measured the overall ability of introductions from either regime to invade into conspecific competitor populations across eight generations. Results showed that populations from stronger sexual selection backgrounds had superior net fitness, invading more rapidly and completely than counterparts from weak sexual selection backgrounds. Despite comprising only 10% of each population at the start of the invasion experiment, colonizations from strong sexual selection histories eventually achieved near‐total introgression, almost completely eliminating the original competitor genotype. Population genetic simulations using the design and parameters of our experiment indicate that this invasion superiority could be explained if strong sexual selection had improved both juvenile and adult fitness, in both sexes. Using a combination of empirical and modeling approaches, our findings therefore reveal positive and wide‐reaching impacts of sexual selection for net population fitness when facing the broad challenge of invading competitor populations across multiple generations.

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“…Theory indicates that when there is strong reproductive skew sexual selection can increase adaptation rates to novel environments: if the skew is in favour of 'high quality' individuals this enhances the spread of adaptive alleles throughout a population (Lorch et al 2003;Mart ınez-Ruiz & Knell 2017). Consistent with this theory, laboratory studies using invertebrate model organisms in experimental evolution designs have found that sexual selection enhances adaptation and protects against extinction (Fricke & Arnqvist 2007;Long et al 2012;Plesnar-Bielak et al 2012;Jacomb et al 2016;Parrett & Knell 2018;Yun et al 2018). Similarly, sexual selection has also been found to enhance the removal of deleterious alleles and to reduce the probability of extinction from inbreeding depression (Jarzebowska & Radwan 2010;Lumley et al 2015).…”

Section: Introductionmentioning

confidence: 98%

Sexual selection predicts the persistence of populations within altered environments

et al. 2019

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The effect of sexual selection on species persistence remains unclear. The cost of bearing ornaments or armaments might increase extinction risk, but sexual selection can also enhance the spread of beneficial alleles and increase the removal of deleterious alleles, potentially reducing extinction risk. Here we investigate the effect of sexual selection on species persistence in a community of 34 species of dung beetles across a gradient of environmental disturbance ranging from old growth forest to oil palm plantation. Horns are sexually selected traits used in contests between males, and we find that both horn presence and relative size are strongly positively associated with species persistence and abundance in altered habitats. Testes mass, an indicator of post‐copulatory selection, is, however, negatively linked with the abundance of species within the most disturbed habitats. This study represents the first evidence from a field system of a population‐level benefit from pre‐copulatory sexual selection.

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Sexual selection expedites the evolution of pesticide resistance

Cited by 27 publications

References 44 publications

The effect of sexual selection on adaptation and extinction under increasing temperatures

The effect of sexual selection on adaptation and extinction under increasing temperatures

Lineages evolved under stronger sexual selection show superior ability to invade conspecific competitor populations

Sexual selection predicts the persistence of populations within altered environments

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