Within-generation and transgenerational social plasticity interact during rapid adaptive evolution

Sturiale, Samantha L; Bailey, Nathan W.

doi:10.1101/2021.10.21.464843

Cited by 4 publications

(4 citation statements)

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“…Conversely, within‐generational plasticity revolves around the individual's proactive sensing or cognition of environmental cues. This perceived information is then synthesized into their environmental interpretations, precipitating a cascade of biochemical, hormonal and molecular responses in phenotypic alterations (Fuxjäger et al., 2019; Sturiale & Bailey, 2023). Finally, it is only the offspring environment that can physically stress an offspring.…”

Section: Discussionmentioning

confidence: 99%

Paternal intergenerational plasticity in the plant species Paeonia ostii: Implications for parental fitness and offspring performance

Zhang,

Ji,

Yao

et al. 2024

Functional Ecology

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While there is long‐standing interest in the role of inter‐ and transgenerational plasticity via the maternal line, it rarely has been studied via the paternal line. Thus, consequences of the paternal environment for parental fitness and for performance of offspring in the environments experienced by either fathers or mothers are not known. We studied the intergenerational plasticity (IGP) of the plant species Paeonia ostii (Paeoniaceae) and tested the hypothesis that exposure of fathers to environmental stress (i) reduces parental fitness and performance of offspring grown under non‐stressful conditions, but (ii) mitigates the negative effects of environmental stress on fitness of parents and performance of offspring. Crosses were made in a greenhouse within six families of P. ostii between parents grown under drought and in a mesic environment, and the offspring of each cross were grown under both dry and mesic conditions. Production and germination of seeds and morphological and physiological traits of offspring were measured as indicators of parental fitness and offspring performance, respectively. Paternal drought decreased seed number per fruit, except when maternal plants also were grown in drought conditions. Offspring drought decreased seedling performance. However, when fathers experienced drought this negative effect on the offspring was partly mitigated, in particular when mothers also had experienced drought. In contrast, offspring grown in mesic conditions had improved seedling performance, especially when either parent (or both) also were grown in mesic conditions. Such statistical differences remained when seed mass was included as a covariate. Overall, paternal pollen of P. ostii mediated IGP to drought almost as well as it did for maternal ovules. IGP was adaptive if environments remained constantly dry across generations but maladaptive if environments changed. Hence, under future climate changes, paternal IGP might be both a blessing and a curse, with the blessing occurring when the focal habitat becomes drier and pollen comes from already‐dry places, while the curse may dominate in predictably moist habitats surrounded by drier habitats. Read the free Plain Language Summary for this article on the Journal blog.

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Section: Discussionmentioning

confidence: 99%

Paternal intergenerational plasticity in the plant species Paeonia ostii: Implications for parental fitness and offspring performance

Zhang,

Ji,

Yao

et al. 2024

Functional Ecology

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“…Additionally, cricket song plays an important role in the social environment, affecting a range of traits such as adult reproductive investment (46), neural gene expression (41), and locomotive activity (47). Should selection against song decrease in severity (e.g., via O. ochracea population decline) in populations in which co-occurrence of Cw and Fw phenotypes has impeded the loss of variation underlying singing-capable male phenotypes, the latter would be expected to once more spread through the population.…”

Section: Discussionmentioning

confidence: 99%

“…The maintenance of non-adaptive variation underlying singing ability in male crickets is of particular evolutionary importance because silent male T. oceanicus benefit from the retention of singing males, which they rely upon to adopt satellite mating tactics (15). Additionally, cricket song plays an important role in the social environment, affecting a range of traits such as adult reproductive investment (46), neural gene expression (41), and locomotive activity (47). Should selection against song decrease in severity (e.g., via O. ochracea population decline) in populations in which co-occurrence of Cw and Fw phenotypes has impeded the loss of variation underlying singing-capable male phenotypes, the latter would be expected to once more spread through the population.…”

Section: Discussionmentioning

confidence: 99%

Competing adaptations maintain non-adaptive variation in a wild cricket population

Rayner,

Eichenberger,

Bainbridge

et al. 2023

Preprint

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How emerging adaptive variants interact is an important factor in the evolution of wild populations. However, the opportunity to empirically study this interaction is rare. We recently documented the emergence of an adaptive phenotype 'curly-wing' in Hawaiian populations of field crickets (Teleogryllus oceanicus). Curly-wing inhibits males' ability to sing, protecting them from eavesdropping parasitoid flies (Ormia ochracea). Surprisingly, curly-wing co-occurs with similarly protective silent 'flatwing' phenotypes in multiple populations, in which neither phenotype has spread to fixation. These two phenotypes are frequently co-expressed, but since either phenotype sufficiently reduces song amplitude to evade the fly, co-expression confers no additional fitness benefit. Numerous negative fitness consequences are known to accompany flatwing, and we find that curly-wing, too, incurs fitness costs via reduced male courtship success and reduced female longevity. We show through crosses, genomic and mRNA sequencing that curly-wing expression is associated with variation on a single autosome. In parallel analyses of flatwing, our results reinforce previous findings of X-linked single-locus inheritance, with the phenotype likely arising through down-regulation of doublesex. By combining insights about the genetic architecture of these alternative phenotypes with simulations and field observations, we show that the co-occurrence of these two adaptations impedes either from fixing, despite extreme fitness benefits. Interestingly, both flatwing and curly-wing are statistically associated with nearby inversions, which are also retained as polymorphisms. This co-occurrence of similar adaptive forms in the same populations might be more common than generally considered, and could be an important force inhibiting adaptive evolution in wild populations.

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“…If the adult B. schlosseri colonies from which larvae were collected experienced a warmer or more variable thermal environment during their lifetime, it may be advantageous for their larvae to exhibit developmental plasticity for temperature tolerance, generating a pattern like that which we found in our study. Reaction norm shape in offspring has been shown to depend in part on parental environment (Salinas et al 2013;Donelson et al 2016;Stein et al 2018;Wadgymar et al 2018;Cavieres et al 2019;Sturiale and Bailey 2021). Despite these examples, the relationship between transgenerational plasticity and within-generation plasticity remains understudied Donelan et al 2020), but interactions between the two could play some role in our observation of increased developmental plasticity at sites with more short-term temperature variability.…”

Section: Potential For Local Adaptation Of Developmental Plasticitymentioning

confidence: 99%

Genomic and physiological adaptation to temperature in the invasive golden star runicate (Botryllus schlosseri)

Tobias

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Because non-indigenous species (NIS) often encounter novel environments during colonization and expansion, species invasions present useful opportunities to investigate the mode and pace of adaptive change in natural populations. In this dissertation, I use the range expansion of the invasive golden star tunicate, Botryllus schlosseri, as a natural experiment to study how a pernicious NIS adapts its thermal physiology on contemporary time scales. In Chapter 2, I applied low-coverage whole genome sequencing (lcWGS) to investigate patterns of population genetic structure and signatures of local adaptation to temperature. In addition to illustrating the potential for rapid adaptation of thermal tolerance at the genomic level, this chapter demonstrated that the molecular basis of thermal adaptation on either coast is distinct, providing valuable evidence for parallel adaptation being driven by divergent molecular means. In Chapter 3, I performed a physiological study to investigate differentiation of post-larval heat tolerance across five populations across a major biogeographic break on the east coast of North America. I found that northern populations are more susceptible to heat stress than their southern, warm-exposed counterparts, providing evidence for adaptive shifts of thermal tolerance. Further, by taking advantage of natural temporal variability in temperature, I demonstrated that temperature during development positively affects heat tolerance at later life stages, establishing developmental plasticity of thermal tolerance. In Chapter 4, I extended my physiological investigation to the west coast of North America, comparing post-larval heat tolerance across three populations spanning a 24.3° latitudinal gradient while expanding to include differentiation of cold tolerance in adults. Similar to the east coast, I observed that the two northern populations were more susceptible to heat stress than their southern counterpart. For cold tolerance, I observed a pattern of countergradient variation whereby northern populations were better able to maintain cardiac function in the cold than southern populations. This suggests compensatory genetic adaptation to the colder water temperatures at higher latitudes. Overall, my work furthers our understanding of how NIS are able to rapidly shift their thermal physiology in response to novel environments, shedding light on the potential of species more generally to adapt to environmental change on contemporary timescales.

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Within-generation and transgenerational social plasticity interact during rapid adaptive evolution

Cited by 4 publications

References 65 publications

Paternal intergenerational plasticity in the plant species Paeonia ostii: Implications for parental fitness and offspring performance

Paternal intergenerational plasticity in the plant species Paeonia ostii: Implications for parental fitness and offspring performance

Competing adaptations maintain non-adaptive variation in a wild cricket population

Genomic and physiological adaptation to temperature in the invasive golden star runicate (Botryllus schlosseri)

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