In a paper published in Biological Reviews in 1970, Geoff Parker reviewed the evidence for sperm competition in nature, discussed why the phenomenon is likely to common in insects and described adaptations in animals to counter sperm competition. Forty-six years after the paper was published I asked Geoff Parker about how he got interested in the topic, the making of this review, and what we have learnt since about sperm competition.
Citation: Parker, G. A. (1970). Sperm competition and its evolutionary consequences in the insects. Biological Reviews, 45(4), 525-567.
Date of interview: Questions sent by email on 18th November 2016; responses received by email on 1st January 2017.
Hari Sridhar: I would like to start by asking you about your motivation to write this paper. From looking at your publication profile, I learnt that you completed your PhD on the reproductive behaviour and the nature of sexual selection in Scatophaga stercoraria L. in 1969. A year later you published this paper. Could you tell us what motivated you to write this paper, in relation to the work you did for your PhD?
Geoff Parker: The last undergraduate research project I completed (in spring 1965) was on the yellow dung fly Scatophaga (in those days, zoology students at Bristol University were expected to submit four research projects in their final year). I continued with this work in October 1965 as the subject of my Ph.D. thesis, which was submitted at the end of September 1968. This certainly inspired the 1970 paper. I was fascinated by the fact that, after mating, a male dung fly guards his female until she has laid all her mature eggs in the cattle dropping. I managed to show that the last male to mate gained most of the eggs the female laid, providing a selective advantage for his mate guarding behaviour. This made me think generally about sperm competition and the suite of adaptations arising from it.
HS: Stepping back a bit, could you tell us how you got interested in insects and Evolutionary Biology? Which came first – an interest in insects or in evolutionary theory?
GP: I had been obsessed with animals and nature in general since very early childhood. Interest in evolution – sensu why animals do what they do – came simultaneously with interest in natural history. Interest in insects and evolution focused in my final year as an undergraduate, when I did two of my research projects on insects, and talked avidly about the mechanism of evolution with fellow student Robin Baker.
HS: Correct me if I’m wrong, but it seems like the phrase “sperm competition” was used for the first time in this paper. Could you share with us the story behind how you came up with the phrase: was this the obvious choice or did you consider other phrases too? Did you spend a lot of time in coming up with the definition? Also, if you were to come up with a phrase and definition today would you word them in the exact same way?
GP: I rather suspect that I wasn’t the first to use this term: I certainly don’t remember thinking much about what term to use. In a paper in 1976 with one of my students, I later tried to change it to ‘ejaculate competition’ (i.e. inter-ejaculate competition) to clearly differentiate it from competition between sperm within the same ejaculate (intra-ejaculate competition).This didn’t catch on, and the term sperm competition has persisted….
HS: Could you give us a sense of the work that went into the making of this paper – did you put together all the literature specifically for the paper, or were you already aware of the literature? Which library did you use for accessing the literature, who were the people you discussed these ideas with etc.?
GP: I had been collecting reprints and references for some time in Bristol before I started to write this paper, which was soon after I arrived at Liverpool University. I had discussed the ideas with Robin Baker and others at Bristol. I didn’t discuss it at Liverpool –in the Zoology Department, we had one embryologist, one neurophysiologist, one parasitologist, etc., so no one would have been particularly interested. However, after the manuscript was written, I do remember phoning Philip Sheppard (then Head of Genetics Department, a remarkably sharp scientist) to finalise details of one of his papers I had cited. Without prompting, he instantly paraphrased some of my main ideas; I was left wondering whether it was a worthwhile project!
HS: Would you remember how long it took you to write up this paper? Also, where and when did you do most of the writing?
GP: I had very little time in my first year at Liverpool to write, since I had a huge teaching load that year (mercifully, this reduced gradually as the years went by). When I could, I vanished to a secluded part of a library to write or access literature, and I worked at home in the evenings and at weekends. Because I had most of the ideas already worked out, the main job was assembling the data from the literature; it did not take long to write. It was one of eight papers written in the first 18 months after I moved to Liverpool – one came out in 1969, and the rest in 1970. Six derived mainly from the thesis, but not the 1970 review.
HS: You acknowledge the help of “Miss D.S. Paterson, Miss G. Robinson and Miss S. Carter” in preparing the manuscript. Could you tell us a little more about who these people were and how they helped?
GP: They were all secretaries, i.e. typists. For preparation and alterations of manuscripts, in those pre-computer days the goodwill of departmental secretaries was essential!
HS: Would you say this paper had a relatively smooth ride through peer-review? Was Biological Reviews the first place it was submitted to?
GP: It went only to Biological Reviews, and was reviewed by the then Editor (Prof. E. Nevill Willmer) and one other reviewer. I looked in my files and found only a long handwritten letter from Prof. Willmer written at his holiday retreat in Wales; he had found it “most interesting”. His main request (and that of the other reviewer) was that it should be shortened to 20,000 words (the submitted version was 25,000 words). I was enthusiastically urged to undertake the revision as quickly as possible. It was a very pleasant, gentlemanly letter. Times have changed!
HS: What kind of attention did this paper receive when it was published? Was it considered controversial at that time?
GP: No – it went virtually unnoticed initially, though both Bob Trivers and Bill Hamilton read it, and were interested. It achieved only a handful of citations for the first few years, and citations increased very gradually over the decades. I think that the topic of sperm competition began to be taken seriously after the symposium in Tucson in 1980, pioneered and arranged by Robert Smith from University of Arizona, resulting in the first monograph on the topic in 1984. He had been working on sperm competition and paternal care in the giant water bug Abedus herberti.
HS: Did this paper have any kind of direct impact on your career? Could you reflect on how it shaped the future course of your research?
GP: Yes, it did; it is certainly the paper I am best known for, and most cited. But I would regard it – and many other areas that I have worked in (e.g. animal contests, sexual conflict, sexual selection, animal distributions, and even the evolution of anisogamy) all as direct or indirect spin-offs from my early field work on yellow dung flies. The 1970s was an incredibly exciting time, when behavioural ecology was just developing: it was immense fun to be a part of all that.
HS: Today, 46 years after it was published, where would you stand on the ideas expressed in this paper? Do you think the ideas and the theory need to be updated in anyway?
GP: I don’t see anything wrong with the major ideas expressed in the 1970 paper, though they have certainly developed enormously since then. By now many books and vast numbers of papers (both empirical and theoretical) have been written on sperm competition and its resultant adaptations. Sperm competition and cryptic female choice have been amalgamated to form the growing field of ‘post-copulatory sexual selection’, which for some reason was not discussed by Darwin, who confined his treatise to pre-copulatory processes.
HS: At the time when you wrote this paper, did you anticipate at all that it would have such a big impact on the field? Also, would you know what the paper mostly gets cited for?
GP: No, I had absolutely no idea that it would have any impact! I was enthusiastic about the review at the time of writing, but would never have guessed that it would become influential. It often gets cited when sperm competition (or post-copulatory sexual selection) is first mentioned in a paper, and often in general reviews on sexual selection and related topics.
HS: You say “Experimental evidence of sperm competition appears to be available for only five orders of insects, and principally for the Diptera” Could you reflect on the extent to which our knowledge of sperm competition has increased today, in insects and other taxa?
GP: At the time, that was probably fairly accurate. By now, sperm competition and its evolutionary consequences have been studied in most animal groups, something I would not have guessed in 1970. One reason for the explosion in sperm competition studies has been the development of modern techniques in molecular biology, which enable paternity to be determined easily (in the past we had to rely on irradiation or the presence of visible genetic markers). There have been extensive studies not only in insects, but also in fishes, birds, mammals and many other taxa. The field of post-copulatory sexual selection is currently rapidly expanding.
HS: You say “In most cases (so far examined) the last male to mate tends to predominate in fertilizing the offspring”. Today, does that view still hold true, in insects and other taxa?
GP: Much depends on the taxon being studied. In some, last male precedence seems to apply, in others, there is something akin to sperm mixing so that paternity follows the raffle (or lottery) principle, in a few the first male appears to predominate.
HS: You say “One of the most fruitful directions for future research may lie in the field of quantitative analyses of adaptive values, which have been attempted much too rarely in the past.” Could you reflect to what extent this has happened in the context of sperm competition, and what lacuna in understanding still remain?
GP: From 1970 onwards, one of the things that the dung fly studies achieved, using optimality/ESS approaches, was to make qualitative predictions about sexually selected adaptations. The fit with observed behaviour was generally very good, which meant that we may have correctly identified the selective forces responsible for shaping the adaptations. The use of detailed, quantitative predictions as a tool for understanding adaptation are still not as common as I should like to see them. Related to this – as to lacunae, we still do not have a great understanding of what selective forces shape the variation in sperm morphology. Although major advances have been made in a few cases, we still are only at the beginning here.
HS: Have you ever read this paper after it was published? If yes, in what context?
GP: Actually no, not completely! But I have delved into it many times to see exactly what I said about particular topics.
HS: Would you count this paper as a favourite, among all the papers you have written?
GP: A favourite, yes; the favourite, no. I think my most important paper is one in 1972 with Robin Baker and Vic Smith on the evolution of anisogamy. I regard it as being more fundamental – it is still probably the best explanation of why there are two sexes. And I would see my 1979 sexual conflict paper (long delayed in press) as being at least as important. But neither of these attracts the citations of the 1970 sperm competition review.
HS: What would you say to a student who is about to read this paper today? What should he or she take away from this paper written 46 years ago? Would you add any caveats?
GP: Unless they were interested in the history of science, I would tell them to ignore the empirical sections and just read the concepts and discussion. So much has been done empirically that they would do better to read something more recent! However, the concepts should still provide a useful introduction to reviews of modern sperm competition theory. The first caveat I would add is to remind them that it was written almost 50 years ago…..The second (given to me long ago by Philip Sheppard) is to get working fast, because they will have had all their best ideas by the time they are 35; after that they will spend their time refining them….
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