Surprising spatiotemporal stability of a multi-peak fitness landscape revealed by independent field experiments measuring hybrid fitness

Martin, Christopher H.; Gould, Katelyn J

doi:10.1002/evl3.195

Cited by 15 publications

(55 citation statements)

References 133 publications

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“…We used linear discriminant axes and generalized additive modelling (GAM) to estimate phenotypic fitness landscapes for the sequenced hybrids on a two-dimensional morphospace indicating similarity to each of the three parental populations following previous studies (17,18).…”

Section: Fitness-associated Snps Improve Inference Of the Adaptive Landscapementioning

confidence: 99%

“…Selection analyses revealed a temporally stable, multi-peaked adaptive landscape across lake populations, year of study, and frequency or density manipulations (Fig. 1B: (17,18,41)). One of the strongest and most persistent trends across studies and treatments was the apparent isolation of hybrid phenotypes resembling the scale-eater by a large fitness valley from the other two species (17,18).…”

Section: Introductionmentioning

confidence: 99%

“…Simpson (7) later described the phenotypic evolution of populations through time on a rugged landscape, in which isolated clusters of fitness peaks represent 'adaptive zones' to which populations evolve from adjacent regions of low fitness (8). Lande and Arnold formalized the analysis of selection and estimation of phenotypic fitness landscapes (9)(10)(11), leading to empirical studies of fitness landscapes in numerous empirical systems (12)(13)(14)(15)(16)(17)(18). Fitness surfaces also provide a central component of speciation models and theory (19)(20)(21).…”

Section: Introductionmentioning

confidence: 99%

“…1B: (17,18,41)). One of the strongest and most persistent trends across studies and treatments was the apparent isolation of hybrid phenotypes resembling the scale-eater by a large fitness valley from the other two species (17,18). Hybrids resembling the generalist occupied a fitness peak and were isolated by a smaller fitness valley from hybrids resembling the molluscivore on a second region of high fitness.…”

Section: Introductionmentioning

confidence: 99%

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Hybridization alters the shape of the genotypic fitness landscape, increasing access to novel fitness peaks during adaptive radiation

Patton

Richards

Gould

et al. 2021

Preprint

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Estimating the complex relationship between fitness and genotype or phenotype (i.e. the adaptive landscape) is one of the central goals of evolutionary biology. Empirical fitness landscapes have now been estimated for numerous systems, from phage to proteins to finches. However, the nature of adaptive walks connecting genotypes to organismal fitness, speciation, and novel ecological niches are still poorly understood. One outstanding system for addressing these connections is a recent adaptive radiation of ecologically and morphologically distinct pupfishes (a generalist, molluscivore, and scale-eater) endemic to San Salvador Island, Bahamas. Here, we leveraged whole-genome sequencing of 139 hybrids from two independent field fitness experiments to identify the genomic basis of fitness, visualize the first genotypic fitness networks in a vertebrate system, and infer the contributions of different sources of genetic variation to the accessibility of the fitness landscape. We identified 132 SNPs that were significantly associated with fitness in field enclosures, including six associated genes that were differentially expressed between specialists, and one gene (protein-lysine methyltransferase: METTL21E) misexpressed in hybrids, suggesting a potential intrinsic genetic incompatibility. We then constructed genotypic fitness networks from adaptive alleles and show that only introgressed and de novo variants, not standing genetic variation, increased the accessibility of genotypic fitness paths from generalist to specialists. Our results suggest that adaptive introgression and de novo variants provided key connections in adaptive walks necessary for crossing fitness valleys and triggering the evolution of novelty during adaptive radiation.

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Section: Fitness-associated Snps Improve Inference Of the Adaptive Landscapementioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Hybridization alters the shape of the genotypic fitness landscape, increasing access to novel fitness peaks during adaptive radiation

Patton

Richards

Gould

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…Diversification on complex adaptive landscapes with multiple empty fitness peaks corresponding to different niches provides an alternative mechanism to niche subdivision and might better explain how a rapid burst of radiation can occur (Kondrashov and Kondrashov 1999; Gavrilets 2004, 2014; Gavrilets and Vose 2005). However, empirical fitness landscapes present the new problem of how populations manage to escape local optima, cross fitness valleys, and access new fitness peaks (Wright 1932; Arnold et al 2001; Burch and Chao 2004; Svennson and Calsbeek 2012; Martin and Wainwright 2013b; Martin 2016; Martin and Gould 2020).…”

Section: Introductionmentioning

confidence: 99%

We get by with a little help from our friends: shared adaptive variation provides a bridge to novel ecological specialists during adaptive radiation

Richards

Martin

2021

Preprint

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Adaptive radiations involve astounding bursts of phenotypic, ecological, and species diversity. However, the microevolutionary processes that underlie the origins of these bursts are still poorly understood. We report the discovery of a cryptic intermediate wide-mouth scale-eating ecomorph in a recent radiation of Cyprinodon pupfishes which provides crucial information about the evolutionary and ecological transition from a widespread algae-eating generalist to a novel microendemic scale-eating specialist. We first show that this ecomorph occurs in sympatry with generalist C. variegatus and scale-eating specialist C. desquamator across several hypersaline lakes on San Salvador Island, Bahamas, but is genetically differentiated, morphologically distinct when reared in a common garden, and sometimes consumes scales. We then compared the timing of selective sweeps on shared and unique adaptive variants in both scale-eating species to characterize the evolutionary path to scale-eating. We predicted that adaptation to the intermediate wide-mouth scale-eating niche aided in the rapid divergence of the more specialized scale-eater C. desquamator. Therefore, selection for shared adaptive variants would occur first in wide-mouth. Contrary to our prediction, four of the six sets of shared adaptive alleles in both scale-eating species swept significantly earlier in C. desquamator. Adaptive introgression from the specialist into the wide-mouth ancestor may have resulted in parallel evolution of their dietary niche. Conversely, no adaptive alleles for scale-eating were reused in a third sympatric specialist C. brontotheriodes, despite sharing 9% of hard selective sweeps. Our work provides a microevolutionary framework for investigating how diversity begets diversity during adaptive radiation.

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Competition-driven eco-evolutionary feedback reshapes bacteriophage lambda’s fitness landscape and enables speciation

Doud,

Gupta,

et al. 2024

Nat Commun

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A major challenge in evolutionary biology is explaining how populations navigate rugged fitness landscapes without getting trapped on local optima. One idea illustrated by adaptive dynamics theory is that as populations adapt, their newly enhanced capacities to exploit resources alter fitness payoffs and restructure the landscape in ways that promote speciation by opening new adaptive pathways. While there have been indirect tests of this theory, to our knowledge none have measured how fitness landscapes deform during adaptation, or test whether these shifts promote diversification. Here, we achieve this by studying bacteriophage $$\lambda$$ λ , a virus that readily speciates into co-existing receptor specialists under controlled laboratory conditions. We use a high-throughput gene editing-phenotyping technology to measure $$\lambda$$ λ ’s fitness landscape in the presence of different evolved-$$\lambda$$ λ competitors and find that the fitness effects of individual mutations, and their epistatic interactions, depend on the competitor. Using these empirical data, we simulate $$\lambda$$ λ ’s evolution on an unchanging landscape and one that recapitulates how the landscape deforms during evolution. $$\lambda$$ λ heterogeneity only evolves in the shifting landscape regime. This study provides a test of adaptive dynamics, and, more broadly, shows how fitness landscapes dynamically change during adaptation, potentiating phenomena like speciation by opening new adaptive pathways.

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Surprising spatiotemporal stability of a multi-peak fitness landscape revealed by independent field experiments measuring hybrid fitness

Cited by 15 publications

References 133 publications

Hybridization alters the shape of the genotypic fitness landscape, increasing access to novel fitness peaks during adaptive radiation

Hybridization alters the shape of the genotypic fitness landscape, increasing access to novel fitness peaks during adaptive radiation

We get by with a little help from our friends: shared adaptive variation provides a bridge to novel ecological specialists during adaptive radiation

Competition-driven eco-evolutionary feedback reshapes bacteriophage lambda’s fitness landscape and enables speciation

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