Social Behaviours: Nurturing nature

Mutant zebrafish exhibit different behaviours depending on the genetic background of the fish they were raised with.
  1. Elena Dreosti  Is a corresponding author
  1. Wolfson Institute for Biomedical Research, University College London, United Kingdom

Behaviours emerge under the combined influence of the environment (nurture) and the genetic information an individual inherited from its ancestors (nature). However, it is still difficult to tease apart the respective contribution of these different factors, which are often deeply intertwined. This is particularly the case with regards to social behaviours.

When animals with a mutation in a gene show a change in a specific behaviour, it is tempting to conclude that said gene is somehow involved in that behaviour. But this is not always the case. Animals are usually raised by their parents and grow up with siblings, who may share the same environment and genetic background (including this mutation). This makes it difficult to pinpoint exactly which elements, or combination of elements, are responsible for the emergence of these ‘behavioural phenotypes’ – that is, behaviours that are associated with a specific genotype.

To understand the direct effect of a specific mutation on the behavioural phenotype of an individual, the environment must be controlled for, including the genetic background of the individual’s social group – its genetic social environment (Baud et al., 2017). Now, in eLife, Rui Oliveira and co-workers based in Portugal, Israel and Poland – including Diogo Ribeiro as first author – report that, in zebrafish, the genetic social environment of an individual while it is growing up affects the adult’s behavioural phenotype (Ribeiro et al., 2020a).

Zebrafish are a good model to study the indirect effects of social genetic variation because they are highly social animals with a genome that can easily be modified. Ribeiro et al. first generated a mutant zebrafish line that lacks the gene for the oxytocin receptor, a protein involved in social-bonding behaviours in animals (Olff et al., 2013). A mutant fish was then either raised with its mutant siblings, or in a group of non-mutant fish. Similarly, a non-mutant individual was raised in a shoal of other non-mutants, or with mutant fish. Using different methods, the team then examined how each combination of genetic and social environment influenced the behavioural phenotype of the mutants.

Regardless of whether they were raised with mutants or non-mutants, fish that lacked the gene for the oxytocin receptor were always worse at discriminating between a familiar and an unfamiliar fish – a result predicted by previous studies (Ribeiro et al., 2020b). However, other experiments revealed that only mutant fish raised with other mutants were more reluctant to approach other fish and to integrate into a shoal. This showed that the genetic background of the group in which mutant fish were raised caused specific social phenotypes, as opposed to the loss of the oxytocin receptor gene alone.

This study may help researchers to understand how the genetic social environment can influence the impact of specific mutations on social interactions. It could also be relevant to work on other forms of behaviour, such as fear conditioning in mice: researchers wishing to investigate this behaviour would normally generate a mouse line lacking a gene thought to be involved in fear conditioning, and then examine how the mutation affects the behaviour of the mice. Variations in fear conditioning in the mutants would then be attributed to the genetic change rather than the social genetic environment. The work of Ribeiro et al. shows that researchers need to be aware of this effect, and control for it whenever possible.

These results also demonstrate the need to be cautious about the many human genetic studies that suggest potential links between a gene and the propensity to develop certain conditions. For instance, the general public now has easy access to DNA tests, which can link variations in certain genes to higher risks of becoming obese, being a smoker, or living a shorter life. However, a gene apparently associated with an increased risk for obesity may in fact be connected to increased parental anxiety. In this case, the weight gain would be a secondary effect of being raised by anxious parents. The impact of the social genetic environment should therefore be carefully assessed for all of these genes.

Finally, Ribeiro et al. show that specific social environments could potentially rescue or promote specific behavioural phenotypes, a finding that could be used to better study human behaviours and socialisation.

References

Article and author information

Author details

  1. Elena Dreosti

    Elena Dreosti is in the Wolfson Institute for Biomedical Research, University College London, United Kingdom

    For correspondence
    e.dreosti@ucl.ac.uk
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6738-7057

Publication history

  1. Version of Record published: September 9, 2020 (version 1)

Copyright

© 2020, Dreosti

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 4,183
    Page views
  • 102
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Elena Dreosti
(2020)
Social Behaviours: Nurturing nature
eLife 9:e61323.
https://doi.org/10.7554/eLife.61323

Further reading

    1. Ecology
    2. Evolutionary Biology
    Nicholas M Grebe, Jean Paul Hirwa ... Stacy Rosenbaum
    Research Article Updated

    Evolutionary theories predict that sibling relationships will reflect a complex balance of cooperative and competitive dynamics. In most mammals, dispersal and death patterns mean that sibling relationships occur in a relatively narrow window during development and/or only with same-sex individuals. Besides humans, one notable exception is mountain gorillas, in which non-sex-biased dispersal, relatively stable group composition, and the long reproductive tenures of alpha males mean that animals routinely reside with both maternally and paternally related siblings, of the same and opposite sex, throughout their lives. Using nearly 40,000 hr of behavioral data collected over 14 years on 699 sibling and 1235 non-sibling pairs of wild mountain gorillas, we demonstrate that individuals have strong affiliative preferences for full and maternal siblings over paternal siblings or unrelated animals, consistent with an inability to discriminate paternal kin. Intriguingly, however, aggression data imply the opposite. Aggression rates were statistically indistinguishable among all types of dyads except one: in mixed-sex dyads, non-siblings engaged in substantially more aggression than siblings of any type. This pattern suggests mountain gorillas may be capable of distinguishing paternal kin but nonetheless choose not to affiliate with them over non-kin. We observe a preference for maternal kin in a species with a high reproductive skew (i.e. high relatedness certainty), even though low reproductive skew (i.e. low relatedness certainty) is believed to underlie such biases in other non-human primates. Our results call into question reasons for strong maternal kin biases when paternal kin are identifiable, familiar, and similarly likely to be long-term groupmates, and they may also suggest behavioral mismatches at play during a transitional period in mountain gorilla society.

    1. Ecology
    2. Evolutionary Biology
    Dakota E McCoy, Benjamin Goulet-Scott ... John Kartesz
    Tools and Resources

    Sustainable cities depend on urban forests. City trees-pillars of urban forests - improve our health, clean the air, store CO2, and cool local temperatures. Comparatively less is known about city tree communities as ecosystems, particularly regarding spatial composition, species diversity, tree health, and the abundance of introduced species. Here, we assembled and standardized a new dataset of N=5,660,237 trees from 63 of the largest US cities with detailed information on location, health, species, and whether a species is introduced or naturally occurring (i.e., 'native'). We further designed new tools to analyze spatial clustering and the abundance of introduced species. We show that trees significantly cluster by species in 98% of cities, potentially increasing pest vulnerability (even in species-diverse cities). Further, introduced species significantly homogenize tree communities across cities, while naturally occurring trees (i.e., 'native' trees) comprise 0.51%-87.3% (median=45.6%) of city tree populations. Introduced species are more common in drier cities, and climate also shapes tree species diversity across urban forests. Parks have greater tree species diversity than urban settings. Compared to past work which focused on canopy cover and species richness, we show the importance of analyzing spatial composition and introduced species in urban ecosystems (and we develop new tools and datasets to do so). Future work could analyze city trees and socio-demographic variables or bird, insect, and plant diversity (e.g., from citizen-science initiatives). With these tools, we may evaluate existing city trees in new, nuanced ways and design future plantings to maximize resistance to pests and climate change. We depend on city trees.