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.
Oxytocin receptor signalling modulates novelty recognition but not social preference in zebrafishJournal of Neuroendocrinology 32:e12834.https://doi.org/10.1111/jne.12834
Groups of animals inhabit vastly different sensory worlds, or umwelten, which shape fundamental aspects of their behaviour. Yet the sensory ecology of species is rarely incorporated into the emerging field of collective behaviour, which studies the movements, population-level behaviours, and emergent properties of animal groups. Here, we review the contributions of sensory ecology and collective behaviour to understanding how animals move and interact within the context of their social and physical environments. Our goal is to advance and bridge these two areas of inquiry and highlight the potential for their creative integration. To achieve this goal, we organise our review around the following themes: (1) identifying the promise of integrating collective behaviour and sensory ecology; (2) defining and exploring the concept of a ‘sensory collective’; (3) considering the potential for sensory collectives to shape the evolution of sensory systems; (4) exploring examples from diverse taxa to illustrate neural circuits involved in sensing and collective behaviour; and (5) suggesting the need for creative conceptual and methodological advances to quantify ‘sensescapes’. In the final section, (6) applications to biological conservation, we argue that these topics are timely, given the ongoing anthropogenic changes to sensory stimuli (e.g. via light, sound, and chemical pollution) which are anticipated to impact animal collectives and group-level behaviour and, in turn, ecosystem composition and function. Our synthesis seeks to provide a forward-looking perspective on how sensory ecologists and collective behaviourists can both learn from and inspire one another to advance our understanding of animal behaviour, ecology, adaptation, and evolution.
Global agro-biodiversity has resulted from processes of plant migration and agricultural adoption. Although critically affecting current diversity, crop diffusion from Classical antiquity to the Middle Ages is poorly researched, overshadowed by studies on that of prehistoric periods. A new archaeobotanical dataset from three Negev Highland desert sites demonstrates the first millennium CE&'s significance for long-term agricultural change in southwest Asia. This enables evaluation of the 'Islamic Green Revolution' (IGR) thesis compared to 'Roman Agricultural Diffusion' (RAD), and both versus crop diffusion during and since the Neolithic. Among the finds, some of the earliest aubergine (Solanum melongena) seeds in the Levant represent the proposed IGR. Several other identified economic plants, including two unprecedented in Levantine archaeobotany-jujube (Ziziphus jujuba/mauritiana) and white lupine (Lupinus albus)-implicate RAD as the greater force for crop migrations. Altogether the evidence supports a gradualist model for Holocene-wide crop diffusion, within which the first millennium CE contributed more to global agricultural diversity than any earlier period.