Reproductive interference in a changing world

Overview

The climate crisis influences us all. Crucially, the ranges of many organisms are shifting – often rapidly – as climate and habitats change. One of the key challenges we face in terms of the climate crisis is predicting how organisms will cope, in particular as shifting ranges generate new species interactions, as previously allopatric populations become sympatric.

In this project, we will examine the evolutionary and ecological consequences of reproductive interference (RI) between two species of seaweed fly, Coelopa frigida and C. pilipes, which are currently undergoing a major range change in the UK and Northern Europe. Reproductive interference describes sexual interactions between two different species, with one or both actors suffering a fitness cost (Shuker & Burdfield-Steel 2017). There has been a resurgence of interest in RI, for instance in terms of its role in both shaping reproductive behaviours and in facilitating the spread of invasive species.

Coelopa frigida and C. pilipes both breed in piles of decomposing seaweed (wrack beds) thrown up above high tide. Both species are found on the coasts of the UK, but over the last three decades both have undergone major range shifts (Edward et al. 2007). Coelopa pilipes was generally restricted to the southern costs of England, but today is found well into Scotland. Indeed, it is now often the most common coelopid on the beaches of Fife. Likewise, C. frigida is now far less common in the south of the UK than it was. Previous work has shown that C. pilipes prefers warmer habitats, both in terms of latitude and even within wrack beds, and is out-competed by C. frigida at lower temperatures.

Whilst we know quite a lot about how temperature influences larval competition and coexistence in these two species (Phillips et al. 1995), we know much less about how reproductive interference may influence ecological competition between them. Moreover, existing evidence for local adaptation in C. frigida (assayed via differences in frequencies of alleles of a polymorphic super-gene, the χβ inversion system), was obtained prior to the changes in ranges of these species, and we do not know whether the rapid range changes will have disrupted patterns of local adaptation in terms of both temperature and inter-specific competition.

Both species are highly promiscuous, and both males and females will mate repeatedly throughout their lives (e.g. Shuker & Day 2001). Whilst inter-specific mating attempts have been observed in the field, we do not yet know how inter-specific interactions between adults, especially in the context of RI, influence fitness, and whether RI is helping or hindering the northerly spread of C. pilipes at the cost of C. frigida.

Methodology

Briefly, the project will involve a series of experimental approaches, in both the laboratory and the field.

We will collect flies of both species from populations in the UK and across Europe with either long or short histories of sympatry, plus a reference population of each species outside historical sympatry. We will perform a series of RI experiments looking at the frequency and costs of mis-directed copulatory attempts, comparing populations of C. frigida and C. pilipes with respect to their experiences of sympatry.

If RI has influenced these species, we would predict that populations with a long history of sympatry will experience (1) less RI, and (2) reduced costs of any mis-placed copulations. On the other hand, populations with only a recent history of sympatry (or no history at all), should experience greater RI and suffer greater costs. If these predictions are correct, then RI may well be shaping how these species interact and their subsequent range changes.

These experiments will then be extended to consider a range of different ambient temperatures, to test whether the effects of RI are influenced by temperature, which might likewise influence how RI helps or hinders range change in these species.

Importantly, we will genotype C. frigida individuals for their χβ inversion karyotype to explore how genetic differences at the χβ super-gene locus influence RI and responses to temperature. Existing SNPs will be used for genotyping.

Seaweed flies can also be sampled and studied in situ, so we will also ground-truth laboratory experiments with behavioural experiments with wild-caught flies at the wrack beds they are collected from. Previous data have shown that both male and female C. frigida retain the high levels of promiscuity seen in the laboratory under these conditions, and we will extend these observations to reproductive interactions between frigida and pilipes.

In addition to asking these rather specific questions about the inter-specific interactions between these two species of seaweed fly, the PhD student may also wish to address fundamental questions about the causes and consequences of RI, using Coelopa as a model system. For instance, how does sexual selection and sexual conflict interact with the environment to shape reproductive interference? Depending on the skills/experience of the successful candidate, there may be opportunities to develop and test mating systems theory in relation to RI. Such theory will help us go back out in the natural world and predict when we might expect RI to influence inter-specific competition and thus shape how species respond to range changes as the global climate shifts.

Project Timeline

Year 1

Population collections; fly husbandry, behaviour and genotyping training; first within- and among species RI experiments. Preparation and publication of review paper exploring potential for range changes bringing about new instances of reproductive interference.

Year 2

On-going lab behavioural experiments; preparation and publication of first behavioural MS. *Possible student placement*

Year 3

Field experiments; on-going lab behavioural experiments, including role of temperature and genotype on RI; scope for novel experiments driven by PhD student and development of new questions/theory; preparation and publication of further behavioural MS (x2-3). *Possible student placement*

Year 3.5

Completion of thesis and MSs.

Training
& Skills

The project will provide a number of key training opportunities: (1) experimental design and behavioural techniques in the lab and field; (2) quantitative skills, from data management through to statistical analysis; (3) molecular biology training, in terms of SNP genotyping; (4) communication skills, to academic, industrial and non-technical audiences.

References & further reading

Edward et al. (2007) Change in the distribution of a member of the strand line community: the seaweed fly (Diptera: Coelopidae). Ecological Entomology 32: 741-746.

Phillips et al. (1995) Coexistence of competing species of seaweed flies: the role of temperature. Ecological Entomology 20: 65-74.

Shuker & Burdfield-Steel (2017) Reproductive interference in insects. Ecological Entomology, 42: 65-75.

Shuker & Day, (2001) The repeatability of a sexual conflict over mating. Animal Behaviour 61: 755-762.

Further Information

We strongly recommend all interested prospective candidates to contact Dr David Shuker (david.shuker@st-andrews.ac.uk) informally to discuss the project and life in the Insect Behavioural Ecology Lab at St Andrews (https://insects.st-andrews.ac.uk).

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