Sperm Biology: An Evolutionary Perspective

Sperm Biology: An Evolutionary Perspective by Tim R.Birkhead, David J.Hosken and Scott S.Pitnick ( eds. ). London : Academic Press . 2008 . 642 pages. Hardback. ISBN 978-0123725684 . £49.99 .

Sperm have long fascinated biologists, although current understanding of their role emerged only gradually. Sperm biology has come a very long way since 1678 when Antonie van Leeuwenhoek first described ‘animalcules’ (spermatozoa) in semen. Nevertheless, despite far-reaching impacts on fundamental evolutionary processes including speciation, and despite a wealth of detailed data from multiple disciplines, an evolutionary synthesis of sperm biology has remained elusive. This edited volume now fills this gap. This is not the result of a one-off meeting of spermatologists, but a mature product founded on a series of biennial meetings, bringing together researchers from a multitude of fields with a common interest in understanding spermatozoa. Written by leading figures, the 15 chapters illuminate key facets of sperm biology, ranging from evolution of this cell type through sperm-egg interactions and speciation to implications for conservation and human fertility.

Chapter 1 provides a comprehensive and enjoyable history, identifying major milestones along the timeline of sperm research. Visualization of sperm requires microscopy, and technological advances that have facilitated and accelerated investigation are outlined. Contributions of key figures are covered, ranging from Leeuwenhoek's initial discovery to Geoff Parker's truly seminal paper defining sperm competition (Parker, 1970). Among other things, it emerges that Leeuwenhoek's understanding of his findings was remarkably close to the truth, much closer than many scientists that followed. For instance, thoughts later drifted into the misguided yet inherently amusing concept of preformation. Surprisingly, it took 200 years before recognition that sperm fused with eggs in the fertilization process became properly established. This instructive chapter sets the scene for subsequent chapters to cover achievements to date. This overview aptly continues in Chapter 2 by evaluating evolutionary forces responsible for origin and maintenance of typical sperm characteristics, e.g. why sperm are smaller and more motile than eggs.

Beyond such basic characteristics, sperm are extraordinarily diverse; this is outlined in Chapter 3 by the editorial triumvirate. As cautioned by the authors, the wealth of data on sperm morphological diversity is mainly descriptive. Understanding the adaptive significance of this variation thus remains a challenge for the future. A close look at sperm from different species uncovers every possible variant imaginable – including sperm without heads or bearing multiple tails, or even giant sperm. Sperm gigantism occurs across the animal kingdom but has been studied most thoroughly in Drosophila where spermatozoa of D. bifurca are 20 times as long as the adult male himself (Bjork & Pitnick, 2006)! As noted here, giant sperm also occur in ostracods. Indeed, recent work using holotomography (permitting visualisation of internal structures of fossils) documents giant sperm in extinct species (Matzke-Karasz et al., 2009). This further underlines the intimate association between technological progress and advances in sperm knowledge.

The next two chapters delve into mechanistic aspects, covering spermatogenesis, sperm motility and energetics. Beyond direct interest to those studying these aspects, this will be useful for researchers investigating postcopulatory sexual selection interested in underlying physiological (or other) mechanisms. Fittingly, Pizzari and Parker then follow through by discussing how sperm competition and selection may have moulded attributes of sperm phenotype (shape, size, motility, etc.). In concluding, the authors suggest going beyond sperm to focus on how spermatozoa and seminal fluid within and between ejaculates interact with the egg and female reproductive tract. A particularly promising route for studying such interactions – as applied successfully in various sexual selection contexts – may be experimental evolution (e.g. Gay et al., 2009).

Emphasizing a theme seen throughout the book, the next two chapters stress how sperm cells should not be viewed solely in isolation. Sperm are adapted for existence outside the male body in the foreign, often hostile, environment of the female tract. Female influences on the fate of sperm are complex and profound. Equally fundamentally, variation in sperm and ejaculate traits in the male governs fertilization success. Male and female reproductive traits bear various marks of coevolution as evidenced by comparative studies (e.g. Minder et al., 2005). Pitnick et al. focus first on interactions of the female with the ejaculate, prompting readers to consider reproduction more broadly than permitted by solely zooming in on single components. Stubbornly attempting to disentangle female- and male-driven processes included in postcopulatory sexual selection might be not merely difficult but also imprudent. Here, too, the merits of experimental evolution allowing targeted manipulation and investigation of sexual selection in action are underlined. Karr, Swanson & Snook then review evolutionary implications of variation in sperm-egg interactions, identifying features common to all animals or restricted to specific taxa. A captivating, meticulous overview details episodes in sperm-egg interactions from first contact to intracellular fertilization. Beyond this, the text encompasses such diverse topics as evolution of sex, reproductive parasites (e.g. the infamous microbe Wolbachia), roles of sperm beyond fertilization, and reproductive isolation.

The material on reproductive isolation links neatly to the next chapter by Howard et al. This clearly written chapter focuses on specific roles played by sperm in speciation, firmly placing the gamete in the limelight of evolution. This will be very welcome to casual readers with broad biological interests. The authors outline numerous examples of post-mating, prezygotic isolation (i.e. focussing on where sperm are critically involved) between closely related species – discussing underlying mechanisms and evolutionary drivers. The involvement of sperm morphology, and interactions with seminal fluid or the egg (signalling, binding) or female tract are described in turn. As evidenced by hybridization and conspecific sperm precedence studies, barriers to gene flow can evolve rapidly and are widespread across the animal kingdom. Predictably, traits involved in gamete recognition evolve especially rapidly (Swanson & Vacquier, 2002).

Simmons and Moore follow by reviewing the quantitative genetics of sperm and provide prospective analyses. They are careful to emphasize that more rigorous analysis would require additional studies. Despite this, useful preliminary summaries are presented (e.g. locations of genes potentially underlying sperm production and performance) and specific pointers for honing future efforts provided (e.g. fine-tuning choice of sperm trait or refining knowledge of genetic architecture). Whereas sperm morphology and function are relatively well described, far less is known of the underlying genetic and molecular basis. This is the subject of the following chapter. Again, further technological advances, this time in genomics and proteomics, have begun to redress this imbalance, as noted in various places throughout the book. For instance, we now have a handle on genes responsible for the proteome, and valuable insights have been gained into genome-level organisation of male reproductive genes and the impact of sexual selection. The authors discuss these findings and conclude that comparative sperm proteomics may be instrumental in exposing the molecular basis of conserved and divergent sperm traits in future.

The following two chapters would probably be best housed in the freak show tent at a spermatology fairground – both display peculiar cases where Mendel's dominion has been toppled. In Chapter 12, Presgraves describes how drive elements acquire more than their fair (Mendelian) share of transmission by partly or fully eliminating competition from alternative gametes. Initially seen as a curiosity, it is now known that such elements are extremely common in eukaryotes (Hurst & Werren, 2001). The most famous elements are t-haplotype in mice and Segregation Distorter in fruit-flies. These are described in detail along with sex ratio distorters, incorporating discussion of underlying genetics, negative impacts on sperm function and implications for sperm competition (see Atlan et al., 2004). This fascinating material is followed by an overview of bizarre gametes and genetics counter to classical, genetically symmetrical systems. The author describes species where cell fusions do not occur in the classical fashion (i.e. between egg and sperm) or where maternal or paternal genomes are excluded.

The penultimate chapter discusses how knowledge of sperm relates to conservation efforts. This is not as substantial as most preceding texts, reflecting the fact that directly relevant data remain sparse. Nevertheless, conserving biodiversity is a burning priority, so future research should focus more on the impact of this and other key reproductive traits on biodiversity. This chapter will suit scientists interested in practical applications of sperm knowledge, e.g. assisted reproduction or fertility consequences of inbreeding. Research assessing effects of inbreeding on reproduction is gathering pace (see Gage et al., 2006). So, as with the speciation chapter, this is topical and of general relevance. Similarly, the final chapter – discussing causes of human infertility, available countermeasures (e.g. IVF) and social implications – will appeal to many, including non-biologists.

To conclude: Well-planned themed primers illuminate many important facets of reproduction with broader implications for fertility or biodiversity, offering something to interest most. The remarkably clear focus on understanding sperm from an evolutionary viewpoint is palpable throughout. As conceded in the preface, there is almost no discussion of gametes in plants or fungi, although key differences between these and animals are briefly mentioned. Parallels between kingdoms have already been drawn (e.g. Till-Bottraud et al., 2005) and further comparisons could be fruitful. This book may well provide the required inspiration. The authors go to great lengths to represent current knowledge of sperm and frequently of eggs. The detailed yet easily accessible chapters are well written and researched, providing extensive overviews of the literature, including up-to-date references. The book as a whole will prove indispensable as a reference work with significance beyond a narrower focus on spermatology. Additionally, numerous highly stimulating research questions are clearly identified throughout. At the end of this journey, readers will undoubtedly realise that sperm are far more complex and interesting than might naively be assumed of such minute cogs in the machinery of reproduction.