BOOK REVIEW

doi:10.1111/j.1558-5646.2009.00930.x

WONDERFUL AND JUST PLAIN WEIRD:THE GLORIOUS BIOLOGY OF SPERMTracey Chapman1,2

1School of Biological Sciences, University of East Anglia, NR4 7TJ, United Kingdom2E-mail: tracey.chapman@uea.ac.uk

Received November 3, 2009

Accepted November 3, 2009

Review of: Sperm Biology: An Evolutionary Perspective. Edited

by Tim R. Birkhead, David J. Hosken, Scott Pitnick, 2009. Else-

vier, Academic Press, Burlington, Massachusetts, 642 pp. ISBN:

9780123725684. $79.95.

From any perspective, sperm are remarkable. We now know

of course that sperm do not contain a tiny version of the adult

(the appealing homunculus imagined by Nicholas Hartsoeker in

the 17th century, Pinto-Correia 1997). Instead, sperm comprise

a head of highly condensed DNA, an acrosome cap, virtually

no cytoplasm, and a long tail partially encased within a sheath

of specialized mitochondria. Then there is their extraordinary

journey, with some sperm cast out into the external environment

and some placed directly within the potentially hostile territory of

the female. Finally, a series of complex processes ensues, leading

to fusion of sperm and egg nuclei and the ultimate formation of

a zygote. What is mind-boggling is how often the situation is

absolutely nothing like the above. Sperm are the most variable

cell type known (Jamieson 1987). They may have no tail or many

tails; possess hooks, coils, spikes, balloons, and other widgets;

vary in the presence of a nucleus, acrosome, and source of fuel

for propulsion. To cap it all even if they are one of the minuscule

percentage of sperm to reach their target, their DNA may still be

ignominiously shoved aside.

In addition to the notable biology, there is obvious interest in

sperm in the context of assisted reproductive technologies in hu-

mans and animals of agricultural and conservation relevance. This

offers an opportunity for a wide-spectrum synthesis, and Sperm

Biology: An Evolutionary Perspective, edited by Tim Birkhead,

David Hosken, and Scott Pitnick fulfils this purpose admirably.

Its aim is to provide a broad evolutionary perspective in a se-

ries of 15 self-contained chapters written by experts across the

whole of animal sperm biology. The book introduces us to its

cast in a photo-autobiographical gallery (surely itself worthy of

further study), and is full of magnificent biology with some ex-

cellent summaries of disparate research areas. It is also thought

provoking in terms of the social context of what can/should be

done in assisted reproduction. It seems somewhat unimaginative

to say that even the bibliography of this book will be useful. But

it really will. Much scholarly research has been done to dig out

diverse literatures and some chapters have useful further reading

suggestions. Most of the book is focused on research conducted

during the last few decades, but that is still an enormous amount of

biology to assimilate. The book is encyclopedic rather than con-

ceptually integrated, and here I aim to highlight the novel themes

and pervasive ideas.

HISTORICAL AND EVOLUTIONARY BEGINNINGS

To start, we are led through three centuries of research into sperm

biology, by Birkhead and Montgomerie. This is a fascinating ac-

count, well written, richly illustrated, and concise. What is nicely

captured here is the dependence of each set of new discoveries

on technological developments, mostly in microscopy. Another

valuable section is on the key players in the history of sperm

research, from Antonie van Leeuwenhoek to Geoff Parker. Hav-

ing softened you up, the book then plunges into the theory on

the fundamental issue—why are sperm small and numerous, and

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BOOK REVIEW

eggs large and few? (Lessells, Snook, and Hosken, Chapter 2).

This gamete size dimorphism is the defining feature of males and

females and a thorough job is done of describing the main ideas:

gamete competition (Parker et al. 1972), sperm limitation (Levitan

1993; Dusenbery 2000), and intracellular conflicts (Cosmides and

Tooby 1981; Hurst 1990). The evolution of size dimorphism re-

quires disruptive selection (separate selection pressures for larger

and smaller size) and negative frequency dependence. The models

overlap to some extent in which of these selection pressures they

invoke, and some models (e.g., gamete competition) appear to

cover more comprehensively the whole of the evolution of sperm

dimorphism than others. A real advantage is that the nuts and

bolts of the models are discussed and compared. Too often the

details of theory are ignored because they are perceived as hard

going, whereas it is surely evident that even abstract models can

have extraordinary explanatory power (Hamilton 1964).

Although theory can give an understanding of the selection

pressures that led to gamete size dimorphism, the actual sequence

of trait evolution is not yet known. It is generally assumed that

isogamy is ancestral, with the evolutionary sequence being the

evolution of different mating types and disassortative gamete fu-

sion, followed by anisogamy and then motility, but this order is

by no means certain (Parker 1978). It seems that there is essen-

tial work to be done to resolve these early sequence transitions,

and here perhaps investigations into the choanoflagellates, the

free-living and flagellated unicellular or colonial organisms that

are considered to be our closest living animal relatives, could be

particularly informative.

A theory-centered approach is also followed by Pizzari and

Parker (Chapter 6) to focus on critical determinants of sperm com-

petition: the number of males in the mating pool, ejaculate quality,

and fertilization efficiency. There has been much investigation of

investment by males into ejaculates in terms of sperm number,

but little attention has been given in this context to the evolution

of sperm phenotype (e.g., sperm longevity, motility). As size also

affects sperm longevity and motility, there may be complex and as

yet unresolved selection pressures at work. The potential conflicts

between the parties involved, male, female, sperm and egg could

even have justified their own chapter.

NEW INSIGHTS INTO SPERM MORPHOLOGY,

SPERMATOGENESIS, AND MOTILITY

Pitnick, Hosken, and Birkhead (Chapter 3) take on the task of

surveying the morphological diversity of sperm. An understand-

ing of some factors that influence sperm morphology has been

gained from comparative data, but explicit theory to explain the

striking morphological diversity of sperm is really lacking. What

I gleaned from this absorbing and beautifully illustrated chapter

was that more or less all sperm characters can vary in the most

spectacular manner, but there is so far no general understanding of

the mechanistic basis, or functional significance of this variation.

Entertainingly, just when you thought the morphology could not

get any more bizarre, the authors themselves opt for a section on

“miscellaneous eccentricities.” However, important broad-scale

insights have emerged: the substantial increase in sperm morpho-

logical diversity following the evolution of internal fertilization

shows that the association with the female reproductive tract has

had a particularly diversifying effect.

Although very little is currently known about the mecha-

nisms that underlie the expression of morphological diversity in

sperm, this will surely change. For example, there is a growing

understanding of the production of dimorphic sperm in Lepi-

doptera, annelid worms, and Drosophila. The two types of sperm

in Lepidoptera are produced from the same primordial sperma-

tocytes, with the switch occurring at meiosis and apyrene (anu-

cleate) sperm taking an abnormal path (e.g., Freidlander 1997).

Some of the hormonal and other factors involved in the devel-

opmental switch are now being identified, which may offer a

valuable opportunity for manipulating the different sperm path-

ways in an experimental context. We might not know much

about the causes of sperm diversity, but a great deal is known

about spermatogenesis itself (Chapter 4, White–Cooper, Doggett,

and Ellis). An excellent summary, it also usefully contrasts be-

tween spermatogenesis and establishment of the germ line in

the mouse, Drosophila melanogaster, and Caenorhabditis ele-

gans. Spermatogenesis within testes is actually evolutionarily

conserved—with the different stages being easily distinguished

across a wide range of taxa.

The adaptive significance of variation in morphology with

respect to the evolution of sperm motility is also currently un-

clear. This important feature of sperm is discussed in Chapter 5

(Cummins). The sperm midpiece is typically thought to provide

the motor for sperm propulsion, and comprises mitochondria sur-

rounding a central axoneme. There is striking variability in mid-

piece size, the number of mitochondria in it, and their arrange-

ment, with insects having a giant mitochondrion formed from the

fusion of many smaller ones. The delivery of ATP from this mo-

tor to the tail is of obvious importance, but many sperm do not

need, or do not rely solely upon, mitochondrially derived ATP and

can instead use the products of glycolysis. There are important

unknowns, such as why some sperm undergo spermiogenesis (ca-

pacitation) and others do not, and also the possible significance

of hyperactivation (which occurs in mammalian sperm) in the

context of sperm competition.

EVOLUTIONARY POTENCY OF INTERACTIONS

BETWEEN EJACULATES AND FEMALES

Until this point we have not heard much about females; this is

remedied by Pitnick, Wolfner, and Suarez (Chapter 7) who dis-

cuss the multifarious interactions between ejaculates and females.

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BOOK REVIEW

This is a huge and scholarly chapter, which claims not to be ex-

haustive but still manages to cite over 400 references. The aim is

to illustrate ejaculate–female interactions (EFIs) and their evolu-

tionary significance by discussing the examples of rapid evolution

and correlated evolution in EFIs before touching on their influ-

ence on traits such as sperm precedence. It is abundantly clear

that ejaculates have significant effects on female behavior and

physiology and that female reproductive tracts also modify com-

ponents of the ejaculate. Rapid evolution in ejaculate proteins

is now well known, but it was nice to see this integrated to-

gether with reproductive morphology. There are far fewer data on

correlated evolution between sperm and the female reproductive

tract. The influence of female reproductive tract morphology on

sperm precedence patterns is a promising topic and can be tested

by artificial selection on female morphology (Miller and Pitnick

2002) and by investigating covariation between sperm competi-

tion dynamics and the morphology of sperm storage organs (e.g.,

Bangham et al. 2003).

SPERM AND EGG INTERACTIONS AND

REPRODUCTIVE ISOLATION

The intimate interactions between sperm and egg (Chapter 8,

Karr, Swanson, and Snook) are discussed in detail in terms of the

key events. Recent research has also revealed that sperm are also

much more than DNA delivery vehicles. Paternal factors delivered

via sperm can affect embryo viability (e.g., Loppin et al. 2005)

and there is also the universal, but so far unexplained, finding that

sperm tails are also fully incorporated within the egg. Collectively

this work is showing that sperm deliver “extra-DNA” structures

and chemicals, and these, together with epigenetic effects, can

significantly alter egg viability and embryonic development. In-

teractions between sperm and egg are of course of central impor-

tance in the evolution of reproductive isolation (Howard, Palumbi,

Birge, and Manier, Chapter 9) and the role played by postmating–

prezygotic (PMPZ) reproductive isolation is discussed. The sig-

nificance of PMPZ in speciation was only realized in the 1990s

because it was previously thought that such barriers did not exist if

hybrids could be formed. However, the discovery of the existence

and strength of conspecific sperm precedence (e.g., Howard 1999)

changed that view. Just because sperm from a different species

can fertilize across the species divide does not mean they actually

do so when conspecific sperm are also present. There are multi-

ple potential mechanisms by which PMPZ barriers could evolve

and evidence for these is discussed in turn, including some of the

authors’ exquisite work on marine invertebrates.

MEIOTIC DRIVE AND CONFLICTS

No story of sperm would be complete without a discussion of the

evolution and operation of drive: the unequal transmission of alle-

les in heterozygotes (Zimmerling et al. 1970). The theory and em-

pirical data on the known autosomal and X-linked drive systems

in mouse, Drosophila, and stalk-eyed flies are laid out concisely,

as well as a synthesis on known mechanisms and adaptations

against driving alleles (Pregraves, Chapter 12). Well-known ex-

amples (segregation distorter, sex ratio, and the t haplotype) were

discovered because of their strong driving effects. What is now be-

coming clear are increasing numbers of cryptic drive mechanisms,

and there are also likely to be many examples where drive is less

strong (and therefore harder to detect) but nevertheless carries a

strong selective advantage. The theme of conflicts is also nicely

extended into discussion of the morphology and role of sperm in

genetic systems other than diplo–diploid (Chapter 13, Normark).

Here, entire paternal genomes are asymmetrically transmitted.

Although a few haplo–diploid lineages have males with relatively

normal sperm, many have sperm that are odd to very odd, often

with markedly elevated numbers of microtubules, although why

is unknown. The conflicts under different genetic systems are dis-

cussed, as are the intriguing ways in which sperm DNA can be

excluded. Examples of purely paternal and maternal inheritance

are now known among the haplo–diploid hymenoptera, including

the recent discovery in the little fire ant that male and female

lineages are mostly separated (Foucaud et al. 2006).

NEGLECTED TECHNIQUES AND NEW TECHNOLOGIES

An attractive addition was the evolutionary quantitative genetics

of sperm (Chapter 10, Simmons and Moore), which is a some-

what neglected field. Studies that examined quantitative genetic

variation in sperm traits are analyzed and summarized. The few

estimates of additive genetic correlations between different sperm

traits are also highlighted, as well as the general lack of mapping

of genes that influence sperm traits. The real surprise is how few

data there are, given that the quantitative genetic methodology

can in principle be relatively easily applied in nonmodel systems.

It seems that there is just not yet the tradition of doing these kinds

of analyses for sperm traits. The potential pay off in terms of

understanding how sperm traits will respond to selection, and de-

tecting the legacy of past selective events, is very high. In terms of

the application of new methodologies, there is also much to learn

from genomic and proteomic techniques (Chapter 11, Dorus and

Karr). The analysis of the D. melanogaster sperm proteome rep-

resents a significant step forward (Dorus et al. 2006) and permits

the first full analysis of sperm protein evolution and rates of di-

vergence, which turn out to be much lower for sperm than for the

seminal fluid medium in which they are transported. It is hard to

see that the whole explanation lies in the relaxation of functional

constraint in nonsperm genes, as many of these are also critical

for fertilization. Perhaps increased degeneracy (as exemplified by

increased levels of gene duplications) within nonsperm genes en-

coding ejaculate components facilitates the more rapid evolution

of new reproductive functions.

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BOOK REVIEW

SPERM AND ASSISTED REPRODUCTION

The book concludes with a discussion of sperm and conservation

(Chapter 14, Roldan and Gomendio) and human fertility and soci-

ety (Chapter 15, Pacey). Given past difficulties in determining fer-

tility parameters in humans (despite the huge industry of research

in this context), we may have some way to go before assisted re-

productive technologies in endangered species can by themselves

offer broad safeguards (Chapter 14). The need to standardize pro-

tocols is an important message: the lack of standard measures has

made it difficult to reliably compare human fertility with that of

even other primates. Troubling variability in semen quality anal-

ysis across different laboratories has also been reported (Matson

1995), leading to categorization of the same individual as either

subfertile or suitable to be a sperm donor. It is obviously impor-

tant, given the strong relationship between sperm concentration

and the probability of pregnancy (Bonde et al. 1998), to get this

right to minimize incorrect intervention and identify when it is

necessary. In addition, reliable estimates of fertility are necessary

to test for fertility declines. Such standardization is essential but

much rarer so far in many other areas of sperm biology. Of much

interest in the context of human fertility and conservation are the

potential dangers of assisted reproduction. These are generally

perceived to be very low, although the longer term risks are not

yet well quantified.

CONCLUSION

This book fills a large gap and will be of interest to a wide

spectrum of biologists, not just those interested in sperm and re-

production, because of its focus throughout on the fundamental

evolutionary principles at work. Guidance in the form of chap-

ter summaries or bullet points (and a contents page with page

numbers) would have been useful, as many of the chapters are

chock full of diverse information. However, overall this book rep-

resents an unusual combination: a valuable academic source that

describes fascinating natural history, bizarre adaptations, and an

unexpectedly large number (to me at any rate) of phenomena of

fascinating but unknown significance.

ACKNOWLEDGMENTSFor valuable discussions, I thank my colleagues and the “book club”: A.Lumley, A. Bourke, A. Millard, C. Fricke, D. Richardson, J. Boone, J.Mason, L. Michalczyk, M. Gage, P. Leftwich, S. Yeates, and S. Diamond.

LITERATURE CITEDBangham, J., T. Chapman, H. K. Smith, and L. Partridge. 2003. Influence of

female reproductive anatomy on the outcome of sperm competition inDrosophila melanogaster. Proc. R. Soc. Lond. B 270:523–530.

Bonde, J. P., E. Ernst, T. K. Jensen, N. H. Hjollund, H. Koslstad, T. B.Henriksen, T. Schieke, A. Giwercman, J. Olsen, and N. E. Skakkebaek.1998. Relation between semen quality and fertility: a population-basedstudy of 430 first pregnancy planners. Lancet 352:1172–1177.

Cosmides, L. M., and J. Tooby. 1981. Cytoplasmic inheritance and intrage-nomic conflict. J. Theor. Biol. 89:83–129.

Dorus, S., S. A. Busby, U. Gerike, J. Shabanowitz, D. F. Hunt, and T. L. Karr.2006. Genomic and functional evolution of the Drosophila melanogaster

sperm proteome. Nat. Genet. 38:1440–1445.Dusenbery, D. B. 2000. Selection for high gamete encounter rates explains

the success of male and female mating types. J. Theor. Biol. 202:1–10.

Foucaud, J., H. Jourdan, J. Le Breton, A. Loiseau, D. Konghouleux, and A.Estoup. 2006. Rare sexual reproduction events in the clonal reproductionsystem of introduced populations of the little fire ant. Evolution 60:1646–1657.

Freidlander, M. 1997. Control of the eupyrene-apyrene sperm dimorphism inLepidoptera. J. Insect Physiol. 43:1085–1092.

Hamilton, W. D. 1964. The genetical evolution of social behaviour I, II. J.Theor. Biol. 7:1–52.

Howard, D. J. 1999. Conspecific sperm and pollen precedence and speciation.Annu. Rev. Ecol. Syst. 30:109–132.

Hurst, L. D. 1990. Parasite diversity and the evolution of diploidy, multicel-lularity and anisogamy. J. Theor. Biol. 144:429–443.

Jamieson, B. G. 1987. The ultrastructure and phylogeny of insect spermatozoa.Cambridge Univ. Press, Cambridge, U.K.

Levitan, D. R. 1993. The importance of sperm limitation to the evolution ofegg size in marine invertebrates. Am. Nat. 141:517–536.

Loppin, B., D. Lepetit, S. Dorus, P. Couble, and T. L. Karr. 2005. Origin andneofunctionalisation of a Drosophila paternal effect gene essential forzygote viability. Curr. Biol. 15:87–93.

Matson, P. L. 1995. External quality assessment for semen analysis and spermantibody detection: results of a pilot scheme. Hum. Reprod. 10:620–625.

Miller, G. T., and S. Pitnick. 2002. Sperm-female coevolution in Drosophila.Science 298:1230–1233.

Parker, G. A. 1978. Selection on non-random fusion of gametes during theevolution of anisogamy. J. Theor. Biol. 73:1–28.

Parker, G. A., V. G. F. Smith, and R. R. Baker. 1972. Origin and evolutionof gamete dimorphism and male-female phenomenon. J. Theor. Biol.36:529–553.

Pinto-Correia, C. 1997. The ovary of eve: egg and sperm preformation. Univ.of Chicago Press, Chicago, IL.

Zimmerling, S., L. Sandler, and B. Nicoletti. 1970. Mechanisms of meioticdrive. Annu. Rev. Genet. 4:409–436.

Book Review Editor: J. Thompson

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