Evolutionary diversity as a catalyst for biological discovery

Johnson, Zachary V.; Young, Larry J.

doi:10.1111/1749-4877.12339

Cited by 22 publications

(19 citation statements)

References 176 publications

(316 reference statements)

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“…However, in the past several years there has been a shift in attention from traditional neuroendocrine approaches, such as hormone manipulation and behavioral pharmacology, toward using genetically modified mouse lines to identify the roles of genes and circuits in regulating behavior with great precision. Often, with what we gain in precision, we lose in diversity and generalizability (Johnson and Young, 2018). We believe that it is imperative to develop state-of-the-art genome manipulation approaches in non-traditional model organisms so that we preserve the advantages of the comparative approach while benefiting from the remarkable power of genetic manipulation.…”

Section: Introductionmentioning

confidence: 99%

Oxytocin receptor knockout prairie voles generated by CRISPR/Cas9 editing show reduced preference for social novelty and exaggerated repetitive behaviors

Horie

Inoue

Suzuki

et al. 2019

Hormones and Behavior

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Behavioral neuroendocrinology has benefited tremendously from the use of a wide range of model organisms that are ideally suited for particular questions. However, in recent years the ability to manipulate the genomes of laboratory strains of mice has led to rapid advances in our understanding of the role of specific genes, circuits and neural populations in regulating behavior. While genome manipulation in mice has been a boon for behavioral neuroscience, the intensive focus on the mouse restricts the diversity in behavioral questions that can be investigated using state-of-the-art techniques. The CRISPR/Cas9 system has great potential for efficiently generating mutants in non-traditional animal models and consequently to reinvigorate comparative behavioral neuroendocrinology. Here we describe the efficient generation of oxytocin receptor (Oxtr) mutant prairie voles (Microtus ochrogaster) using the CRISPR/Cas9 system, and describe initial behavioral phenotyping focusing on behaviors relevant to autism. Oxtr mutant male voles show no disruption in pup ultrasonic vocalization, anxiety as measured by the open field test, alloparental behavior, or sociability in the three chamber test. Mutants did however show a modest elevation in repetitive behavior in the marble burying test, and an impairment in preference for social novelty.

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Section: Introductionmentioning

confidence: 99%

Oxytocin receptor knockout prairie voles generated by CRISPR/Cas9 editing show reduced preference for social novelty and exaggerated repetitive behaviors

Horie

Inoue

Suzuki

et al. 2019

Hormones and Behavior

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“…Since the pioneering study of maternal behavior induced by centrally administered oxytocin (OT) in virgin rats [22], studies have been conducted to investigate how the evolutionarily conserved OT modulates reciprocal interactions among individuals in each species of vertebrates [23,24,25]. In humans, many studies have focused on social cognition and prosociality promoted by OT in interpersonal relationships in typically developing individuals [26,27,28,29].…”

Section: Introductionmentioning

confidence: 99%

Social Interaction Improved by Oxytocin in the Subclass of Autism with Comorbid Intellectual Disabilities

et al. 2019

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Approximately half of all autism spectrum disorder (ASD) individuals suffer from comorbid intellectual disabilities. Furthermore, the prevalence of epilepsy has been estimated to be 46% of patients with low intelligence quotient. It is important to investigate the therapeutic benefits and adverse effects of any recently developed drugs for this proportion of individuals with the so-called Kanner type of ASD. Therefore, we investigated the therapeutic and/or adverse effects of intranasal oxytocin (OT) administration, especially in adolescents and adults with ASD and comorbid intellectual disability and epilepsy, with regard to core symptoms of social deficits. We have already reported three randomized placebo-controlled trials (RCTs). However, we revisit results in our pilot studies from the view of comorbidity. Most of the intellectually disabled participants were found to be feasible participants of the RCT. We observed significantly more events regarded as reciprocal social interaction in the OT group compared with the placebo group. In the trial, no or little differences in adverse events were found between the OT and placebo arms, as found in some other reports. However, seizures were induced in three participants with medical history of epilepsy during or after OT treatment. In conclusion, we stress that behavioral changes in ASD patients with intellectual disabilities could be recognized not by the conventional measurements of ASD symptoms but by detailed evaluation of social interactions arising in daily-life situations.

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“…Animal models for human disease have been restricted to a few species. However, evolution has generated species that display a wide range of phenotypic diversity, the study of some of which may provide novel insight into the causes of human behaviors (Johnson and Young, 2018). Astyanax mexicanus has previously been proposed as a model for evolutionary medicine for understanding traits relevant to human health and disease, including retinal degeneration and insulin resistance (Albertson et al, 2009;Krishnan and Rohner, 2019).…”

Section: Evolutionary Medicinementioning

confidence: 99%

Utilizing the blind cavefish Astyanax mexicanus to understand the genetic basis of behavioral evolution

Kowalko

2020

Journal of Experimental Biology

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Colonization of novel habitats often results in the evolution of diverse behaviors. Comparisons between individuals from closely related populations that have evolved divergent behaviors in different environments can be used to investigate behavioral evolution. However, until recently, functionally connecting genotypes to behavioral phenotypes in these evolutionarily relevant organisms has been difficult. The development of gene editing tools will facilitate functional genetic analysis of genotype-phenotype connections in virtually any organism, and has the potential to significantly transform the field of behavioral genetics when applied to ecologically and evolutionarily relevant organisms. The blind cavefish Astyanax mexicanus provides a remarkable example of evolution associated with colonization of a novel habitat. These fish consist of a single species that includes sighted surface fish that inhabit the rivers of Mexico and southern Texas and at least 29 populations of blind cavefish from the Sierra Del Abra and Sierra de Guatemala regions of Northeast Mexico. Although eye loss and albinism have been studied extensively in A. mexicanus, derived behavioral traits including sleep loss, alterations in foraging and reduction in social behaviors are now also being investigated in this species to understand the genetic and neural basis of behavioral evolution. Astyanax mexicanus has emerged as a powerful model system for genotype-phenotype mapping because surface and cavefish are interfertile. Further, the molecular basis of repeated trait evolution can be examined in this species, as multiple cave populations have independently evolved the same traits. A sequenced genome and the implementation of gene editing in A. mexicanus provides a platform for gene discovery and identification of the contributions of naturally occurring variation to behaviors. This review describes the current knowledge of behavioral evolution in A. mexicanus with an emphasis on the molecular and genetic underpinnings of evolved behaviors. Multiple avenues of new research that can be pursued using gene editing tools are identified, and how these will enhance our understanding of behavioral evolution is discussed.

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Evolutionary diversity as a catalyst for biological discovery

Cited by 22 publications

References 176 publications

Oxytocin receptor knockout prairie voles generated by CRISPR/Cas9 editing show reduced preference for social novelty and exaggerated repetitive behaviors

Oxytocin receptor knockout prairie voles generated by CRISPR/Cas9 editing show reduced preference for social novelty and exaggerated repetitive behaviors

Social Interaction Improved by Oxytocin in the Subclass of Autism with Comorbid Intellectual Disabilities

Utilizing the blind cavefish Astyanax mexicanus to understand the genetic basis of behavioral evolution

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