measure for measure: female responses to the social and sexual environment.

Lead Research Organisation: University of East Anglia
Department Name: Biological Sciences

Abstract

We respond to our environments in all sorts of ways, generally to fit in or become more competitive - such responses are usually beneficial, though can also be expressed in a pathological manner as so-called 'gang' or 'lad' culture. As an example of a social / sexual response, we may often adopt the speech patterns or mannerisms of the people we are talking to in an unknowing effort to ease communication. The animal world is full of analogous examples. Males in groups perceive that they are under a potentially elevated risk of competition for mates and matings. Hence such males may compete more strongly for matings, elevate their courtship rituals, mate for longer and transfer more sperm and ejaculate proteins when they do mate. These effects have been shown to benefit males that are subject to reproductive competition by allowing them to increase their investment in reproduction when it is relevant to do so.

Our work shows that females also show substantial variation in responses to males, mating and sexual context. However, virtually nothing is yet known about the significance of these responses. Unlike for males, we do not know the benefits of responding to the sexual environment, nor what the consequences are for the female's offspring. This is especially important as parental social experience can influence offspring performance through non-genetic effects. Hence mothers may be able to 'prepare' their offspring for the prevailing competitive environment.

Hence, we conclude that both sexes can express considerable plasticity in responses to the environment, which offers much raw material upon which natural selection can act. Yet the significance of all this genetic variation remains a mystery.

In addition, given that both sexes can exhibit reproductive plasticity (e.g. in how much investment to make in each reproductive episode) it is surprising that we don't yet know what the sum contribution of these effects is to an individual's overall reproductive success. When both mating partners are in agreement with one another over reproductive decisions, then '2 partner plasticity' should increase overall reproductive success. However, if there is conflict, as there often is, then the benefits of plasticity expressed by each partner may cancel each other out.

All these ideas have never previously been tested.

We propose here a highly novel research programme to tackle big gaps in our understanding of sexual plasticity in females. We will use fully genome-sequenced 'iso-female' lines. These offer the potential to measure the extent of genetic variation in each of the experiments we will conduct and, in the future, to pin down the genome regions associated with each reproductive character in much the same way as tests of genes 'for' specific diseases are conducted by medical researchers.

We have 3 broad aims:

1. To measure the benefits for females of expressing reproductive plasticity.
2. To discover whether females can signal the likely competitive environment into which their male and female offspring will emerge.
3. To discover how the plastic responses of male and females interact.

The results will contribute significantly to our fundamental understanding of reproductive decisions made by males and females. They will also reveal the mechanisms by which females can sense competition and signal competitiveness to future generations.

Planned Impact

The proposed work is expected to generate significant impacts - we describe below who will benefit and the mechanisms in place to show how that impact will be achieved.

1. DISSEMINATION OF FUNDAMENTAL SCIENCE ACROSS ACADEMIC AND PUBLIC DOMAINS: A wealth of data on the different facets of plasticity in different environments will be generated. These data are expected to be the springboard for further future studies by us and by other researchers. These impacts will be delivered by the PI, Researcher Co-I and Co-I through published papers, press releases, science blogs, twitter, conferences and reports. Public dissemination will be achieved through the whole team via the diverse outreach and engagement activities specified in the pathways plan. Collectively we have a strong record in such activities (local and national public exhibitions such as at the Royal Society, Norwich Forum, Sainsbury Centre for Visual Arts, blogging and twitter). We see several possibilities for research outcomes to gain the attention of a broad audience:

(i) Sexual plasticity: there are strong potential impacts arising from understanding basic processes such as who mates with who, why and the resulting consequences. This impact will be disseminated to researchers in this field using the research expertise and research links of the whole team.

(ii) Divergence: ultimately we wish to understand the role of plasticity in females and males in contributing to evolutionary change - in this project we will identify the processes underpinning such processes. This information should prove important in terms of both public impact and further research in this area, especially given the opportunity to manipulate different sets of genes in order to start to probe causality (and thus ultimately to identify the gene regions responsible). Theory reveals the likely role of both males and female plasticity in contributing to phenotypic variation. Our experiments should yield important additional anchoring data for those studies. The PI and Co-Is will drive this potential impact through public exhibitions and talks, with which they have a good level of experience.

(iii) Divergent reproductive strategies: we will gain much needed information on differences in female responses to their environments. This impact is expected to be realised in the public domain through its intrinsic interest and via our mechanisms for engagement.

2. NOVEL METHODS OF INSECT CONTROL. The proposed work is relevant to the potential for understanding, manipulating and improving the sexual performance of mass-reared insects subject to mass release programmes for control. Our data will highlight mechanisms by which individuals can respond their environments and identify new candidate loci that could be manipulated for control. We have strong links with the applied insect research community (PI in PhD projects with Oxitec, Pirbright and Ecospray Ltd). To elaborate: the PI has previously held 2 NERC iCASE PhD studentships with Oxford Insect technologies (Oxitec Ltd), two more CASE studentships started in Oct 2015 (Institute of Animal Health and a further industry-funded PhD studentship with Oxitec). Oxitec were also a Project Partner on a BBSRC grant BB/K000489/1. These active, ongoing relationships have cemented relevant industry contacts and strong research links to the applied community.
 
Description So far on this new project we have discovered that females are every bit as responsive as are males to their social and sexual context. Females that exposed to other females prior to mating are slower to mate. We are currently testing whether this is an effect of exposure to females / males of the same / closely-related species, specifically. The results are interesting in the context of whether females respond to competition per se or to food / oviposition site availability.

We discovered that females secrete public goods on their eggs, leading to follow up funding NE/T007133/1 from NERC. We also now know the cues used by fermales to respond to each other and are preparing that work for submission to Current Biology.

The following publications are arising:

Rostant WR, Fowler EK & Chapman T. (2020) Sexual conflict theory: concepts and empirical tests. The SAGE Handbook of Evolutionary Psychology, edited by Todd Shackelford, in press.

Fowler EK, Bradbury T, Moxon S, Chapman T. (2019) Sex-specific transcriptional responses to mating in D. melanogaster. Scientific Reports in press.

Dore AA, Bretman A & Chapman T. (2020) Fitness consequences of redundant cues of competition in male D. melanogaster. Ecology and Evolution, accepted.

Dore AA, Rostrant WG, Bretman A & Chapman T. Plastic male mating behaviour evolves in response to the competitive environment. Submitted to Nature Ecology and Evolution.
Exploitation Route To improve insect husbandry for pest insect control, potentially. As a novel test of social evolution theory, as indicated by the successful award of follow up research grant funding.
Sectors Agriculture, Food and Drink,Environment

 
Description BBSRC DTP studentship to T Chapman and W Haerty on sexual detection - social responses in fruitflies
Amount £100,000 (GBP)
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 10/2019 
End 09/2023
 
Description NERC standard discovery research grant
Amount £800,000 (GBP)
Funding ID NE/T007133/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 09/2020 
End 08/2023