Genetic variance in fitness indicates rapid contemporary adaptive evolution in wild animals

Bonnet, Timothée; Morrissey, Michael B.; Villemereuil, Pierre de; Alberts, Susan C.; Arcese, Peter; Bailey, Liam D.; Boutin, Stan; Brekke, Patricia; Brent, Lauren J. N.; Camenisch, Glauco; Charmantier, Anne; Clutton‐Brock, Tim; Cockburn, Andrew; Coltman, David W.; Courtiol, Alexandre; Davidian, Eve; Evans, Simon; Ewen, John G.; Festa-Bianchet, Marco; Franceschi, Christophe de; Gustafsson, Lars; Höner, Oliver P.; Houslay, Thomas M.; Keller, Lukas F.; Manser, Marta B.; McAdam, Andrew G.; McLean, Emily; Nietlisbach, Pirmin; Osmond, Helen L.; Pemberton, Josephine M.; Postma, Erik; Reid, Jane M.; Rutschmann, Alexis; Santure, Anna W.; Sheldon, Ben C.; Slate, Jon; Teplitsky, Céline; Visser, Marcel E.; Wachter, Bettina; Kruuk, Loeske E. B.

doi:10.1126/science.abk0853

Cited by 100 publications

(82 citation statements)

References 221 publications

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“…These data, in combination, are key for studying the evolution of sociality. Extensive pedigrees have been used to look at, as examples, the contribution of additive genetic effects to the gut microbiome (Grieneisen et al 2021 ) and for estimating rates of contemporary adaptive evolution in wild animal populations (Bonnet et al 2022 ). We hope that other long-term field studies join in further investigating the relative importance of genetic versus non-genetic effects in driving variation in sociality, as this information is crucial to understanding how a population can respond to selection and thus the potential for adaptive evolution in sociality.…”

Section: Discussionmentioning

confidence: 99%

Genetic, maternal, and environmental influences on sociality in a pedigreed primate population

2022

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Various aspects of sociality in mammals (e.g., dyadic connectedness) are linked with measures of biological fitness (e.g., longevity). How within- and between-individual variation in relevant social traits arises in uncontrolled wild populations is challenging to determine but is crucial for understanding constraints on the evolution of sociality. We use an advanced statistical method, known as the ‘animal model’, which incorporates pedigree information, to look at social, genetic, and environmental influences on sociality in a long-lived wild primate. We leverage a longitudinal database spanning 20 years of observation on individually recognized white-faced capuchin monkeys (Cebus capucinus imitator), with a multi-generational pedigree. We analyze two measures of spatial association, using repeat sampling of 376 individuals (mean: 53.5 months per subject, range: 6–185 months per subject). Conditioned on the effects of age, sex, group size, seasonality, and El Niño–Southern Oscillation phases, we show low to moderate long-term repeatability (across years) of the proportion of time spent social (posterior mode [95% Highest Posterior Density interval]: 0.207 [0.169, 0.265]) and of average number of partners (0.144 [0.113, 0.181]) (latent scale). Most of this long-term repeatability could be explained by modest heritability (h2social: 0.152 [0.094, 0.207]; h2partners: 0.113 [0.076, 0.149]) with small long-term maternal effects (m2social: 0.000 [0.000, 0.045]; m2partners: 0.000 [0.000, 0.041]). Our models capture the majority of variance in our behavioral traits, with much of the variance explained by temporally changing factors, such as group of residence, highlighting potential limits to the evolvability of our trait due to social and environmental constraints.

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Section: Discussionmentioning

confidence: 99%

Genetic, maternal, and environmental influences on sociality in a pedigreed primate population

2022

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“…The field of conservation genetics has its roots in understanding the genetic and evolutionary mechanisms that negatively affect small and threatened populations, such as inbreeding, random genetic drift, and genetic load (Frankham et al, 2010). More recently, there has been greater recognition of the importance of genetic variation in facilitating adaptation and resilience to change (Hoffmann et al, 2021, Bonnet et al, 2022). We argue here that we now need to consider further how we can harness evolutionary processes (evolutionary adaptation) to enable the coexistence of native prey and invasive predators.…”

Section: Essaymentioning

confidence: 99%

Coexistence conservation: Reconciling threatened species and invasive predators through adaptive ecological and evolutionary approaches

Evans

Weeks

Scheele

et al. 2022

Conservat Sci and Prac

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Invasive predators are responsible for declines in many animal species across the globe. To redress these declines, conservationists have undertaken substantial work to remove invasive predators or mitigate their effects. Yet, the challenges associated with removal of invasive predators mean that most successful conservation programs have been restricted to small islands, enclosures (“safe havens”), or refuge habitats where threatened species can persist. While these approaches have been, and will continue to be, crucial for the survival of many species, in some contexts they may eventually lock in a baseline where native species vulnerable to invasive predators are accepted as permanently absent from the wild (shifting baseline syndrome). We propose an explicit theme in conservation biology termed “coexistence conservation,” that is distinguished by its pursuit of innovative solutions that drive or enable adaptive evolution of threatened species and invasive predators to occur over the long term. We argue evolution has a large role to play but using it to adapt native species to a new environmental order requires a shift in mindset from small, isolated, and short‐term leaps to deliberate, staged steps within a long‐term strategy. A key principle of coexistence conservation is that predation is treated as the threat, rather than the predator, driving a focus on the outcome rather than the agent. Without a long‐term strategy, we face the permanent loss of many species in the wild. Coexistence conservation is a complementary approach to current practice and will play an important role in shifting our current trajectory from continued and rapid invasive predator‐driven defaunation to a world where invasive predators and native prey can coexist.

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“…The Tiritiri Mātangi and Kārori populations (the two populations of interest) occur at the two extremes of this range (i.e., the sanctuaries are 525 kms apart), with hihi monitored since reintroduction and lay date and reproductive success consistently recorded for both populations. Previous studies have demonstrated that both populations contain low levels of genetic diversity (Brekke et al, 2011;de Villemereuil, Rutschmann, Lee, et al, 2019), low levels of additive genetic variance and therefore a low adaptive potential (Bonnet et al, 2022;Rutschmann et al, 2020). This low ability to adapt for hihi is in contrast to other species where higher adaptive potential has enabled a shift towards earlier lay dates in response to climate change (Charmantier & Gienapp, 2014; for a New Zealand species see: Teplitsky et al, 2010).…”

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confidence: 99%

Variation in shape and consistency of selection between populations of the threatened Hihi (Notiomystis cincta)

Rutschmann

Santure

Brekke

et al. 2022

J of Evolutionary Biology

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The shape and intensity of natural selection can vary between years, potentially resulting in a chronic reduction of fitness as individuals need to track a continually changing optimum of fitness (i.e., a “lag load”). In endangered species, often characterized by small population size, the lack of genetic diversity is expected to limit the response to this constant need to adjust to fluctuating selection, increasing the fitness burden and thus the risk of extinction. Here, we use long‐term monitoring data to assess whether the type of selection for a key fitness trait (i.e., lay date) differs between two reintroduced populations of a threatened passerine bird, the hihi (Notiomystis cincta). We apply recent statistical developments to test for the presence or absence of fluctuation in selection in both the Tiritiri Mātangi Island and the Kārori sanctuary populations. Our results support the presence of stabilizing selection in Tiritiri Mātangi with a potential moving optimum for lay date. In Kārori our results favour a regime of directional selection. Although the shape of selection may differ, for both populations an earlier lay date generally increases fitness in both environments. Further, the moving optimum models of lay date on Tiritiri Mātangi, suggesting that selection varies between years, imply a substantial lag load in addition to the fitness burden caused by the population laying too late. Our results highlight the importance of characterizing the form and temporal variation of selection for each population to predict the effects of environmental change and to inform management.

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Genetic variance in fitness indicates rapid contemporary adaptive evolution in wild animals

Cited by 100 publications

References 221 publications

Genetic, maternal, and environmental influences on sociality in a pedigreed primate population

Genetic, maternal, and environmental influences on sociality in a pedigreed primate population

Coexistence conservation: Reconciling threatened species and invasive predators through adaptive ecological and evolutionary approaches

Variation in shape and consistency of selection between populations of the threatened Hihi (Notiomystis cincta)

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