Does Behavior Evolve First? Correlated Responses to Selection for Voluntary Wheel-Running Behavior in House Mice

Khan, Rahim H.; Rhodes, Justin S.; Girard, Isabelle A.; Schwartz, Nicole E.; Garland, Theodore

doi:10.1086/730153

Cited by 7 publications

(3 citation statements)

References 148 publications

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“…Alterations in the transcriptome also indicates changes in olfactory and vomeronasal systems [ 48 ]. Taken together, these results indicate that perception of smell may be a notable factor in their motivation for running on the wheels and also consistent with the idea that motivation is expected to evolve before ability [ 20 , 73 ]. Interestingly, although both generations demonstrate evolution in genomic regions association with olfaction and vomeronasal, the regions implicated in each generation are different, with exception of the region on chromosome 14 (chr14:52,115,206–53,776,455), which was identified by the generation 22 WRT analyses and the generation 61 mixed model analyses ( Table 2 ).…”

Section: Discussionsupporting

confidence: 84%

“…Roughly 10 male and 10 female mice were taken from each line at generation 22 [ 20 ]. Mice were decapitated without anesthesia because blood was being taken for a study of hormone levels (corticosterone) that can respond rapidly to additional handling or anesthesia.…”

Section: Methodsmentioning

confidence: 99%

“…Numerous physiological and morphological differences between the HR and control lines have been documented [ 16 – 20 ]. These include traits associated with motivation to run, such as changes in dopamine [ 21 , 22 ], serotonin [ 23 ], and endocannabinoid signaling [ 24 ], as well as changes in brain size and structure [ 25 ].…”

Section: Introductionmentioning

confidence: 99%

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Large changes in detected selection signatures after a selection limit in mice bred for voluntary wheel-running behavior

Hillis,

Yadgary,

Weinstock

et al. 2024

PLoS ONE

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In various organisms, sequencing of selectively bred lines at apparent selection limits has demonstrated that genetic variation can remain at many loci, implying that evolution at the genetic level may continue even if the population mean phenotype remains constant. We compared selection signatures at generations 22 and 61 of the “High Runner” mouse experiment, which includes 4 replicate lines bred for voluntary wheel-running behavior (HR) and 4 non-selected control (C) lines. Previously, we reported multiple regions of differentiation between the HR and C lines, based on whole-genome sequence data for 10 mice from each line at generation 61, which was >31 generations after selection limits had been reached in all HR lines. Here, we analyzed pooled sequencing data from ~20 mice for each of the 8 lines at generation 22, around when HR lines were reaching limits. Differentiation analyses of allele frequencies at ~4.4 million SNP loci used the regularized T-test and detected 258 differentiated regions with FDR = 0.01. Comparable analyses involving pooling generation 61 individual mouse genotypes into allele frequencies by line produced only 11 such regions, with almost no overlap among the largest and most statistically significant peaks between the two generations. These results implicate a sort of “genetic churn” that continues at loci relevant for running. Simulations indicate that loss of statistical power due to random genetic drift and sampling error are insufficient to explain the differences in selection signatures. The 13 differentiated regions at generation 22 with strict culling measures include 79 genes related to a wide variety of functions. Gene ontology identified pathways related to olfaction and vomeronasal pathways as being overrepresented, consistent with generation 61 analyses, despite those specific regions differing between generations. Genes Dspp and Rbm24 are also identified as potentially explaining known bone and skeletal muscle differences, respectively, between the linetypes.

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Section: Discussionsupporting

confidence: 84%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Large changes in detected selection signatures after a selection limit in mice bred for voluntary wheel-running behavior

Hillis,

Yadgary,

Weinstock

et al. 2024

PLoS ONE

Self Cite

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Osteocyte Sptbn1 Deficiency Alters Cell Survival and Mechanotransduction Following Formation of Plasma Membrane Disruptions (PMD) from Mechanical Loading

Hagan,

Tuladhar,

et al. 2024

Calcif Tissue Int

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Can a Hybrid Line Break a Selection Limit on Behavioral Evolution in Mice?

Hiramatsu,

Careau,

Garland

2024

Behav Genet

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Artificial selection yielded four replicate high runner (HR) lines of mice that reached apparent selection limits (~ threefold increase in wheel revolutions per day vs. four control lines), despite maintenance of additive genetic variance. After 68 generations, we used animal models to test for changes in additive-genetic variances and covariance of the two measured components (average speed and duration) of running distance. We also attempted to break the selection limit by crossing two HR lines, then continuing directional selection on this hybrid line and on the two parental lines for nine generations. The genetic correlation between speed and duration was positive in the base population, but evolved to be negative in the two parental HR lines. Although heritability for both speed and duration (but not distance) increased in the hybrid line, their genetic correlation remained negative. Hybrid F1 mice from generation 68 parents showed heterosis for running distance, which was lost in subsequent generations, and the hybrid line did not exceed the limit. Both male and female hybrids ran faster than parental lines for most generations, but running duration was intermediate or reduced, reflecting their negative genetic correlation. The evolved genetic trade-off between speed and duration may explain the inability for the hybrid line to break the selection limit for distance run, despite renewed additive genetic variance for at least one of its component traits.

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Does Behavior Evolve First? Correlated Responses to Selection for Voluntary Wheel-Running Behavior in House Mice

Cited by 7 publications

References 148 publications

Large changes in detected selection signatures after a selection limit in mice bred for voluntary wheel-running behavior

Large changes in detected selection signatures after a selection limit in mice bred for voluntary wheel-running behavior

Osteocyte Sptbn1 Deficiency Alters Cell Survival and Mechanotransduction Following Formation of Plasma Membrane Disruptions (PMD) from Mechanical Loading

Can a Hybrid Line Break a Selection Limit on Behavioral Evolution in Mice?

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