Cryptic Female Choice
Hanne Løvlie
Linköping University Post Print
N.B.: When citing this work, cite the original article.
The original publication is available at www.springerlink.com:
Hanne Løvlie, Cryptic Female Choice, 2016, Evolutionary biology.
http://dx.doi.org/10.1093/OBO/9780199941728-0071
Copyright: Springer Verlag (Germany)
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Postprint available at: Linköping University Electronic Press
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Cryptic female choice
Hanne Løvlie
Linköping University
Introduction
General overviews
Journals
Definition and history
When to expect cryptic female choice
Potential pitfalls in the study of cryptic female choice
Some useful techniques
Artificial insemination
Florescent protein labelling of sperm prior to insemination
Counting sperm in female sperm storage organs
Genotyping of sperm in female sperm storage organs
Counting the number of hydrolysis points on the perivitelline layer of eggs
Female benefits from cryptic female choice
Direct benefits
Indirect benefits
Good sperm
Sexy sperm
Compatible sperm
Mechanisms and processes used as cryptic female choice
Copulation courtship
Female control of oviposition
Female reproductive tract morphology
Female removal of spermatophore or copulatory plug
Female ejaculate ejection or sperm dumping
Female control of sperm storage
Female reproductive tract-ejaculate interactions
Ovarian fluid differentially affecting sperm
Sperm-egg interactions
Post-insemination pre-fertilisation female bias
Cryptic female choice in plants
Theoretical models including cryptic female choice
Introduction
Sexual selection (Oxford Bibliographies article *‘Sexual selection’ by Kvarnemo) is a powerful
evolutionary force, selecting for traits that increase the reproductive success of individuals. Before
copulation, sexual selection can occur through intra-sexual selection typically observed as
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competition among individuals of the same sex for access to mating partners of the other sex (Oxford
Bibliographies article *‘Male-male competition’ by Miller & Somjee), and inter-sexual selection
observed as (typically female) mate choice (Oxford Bibliographies article *‘Mate Choice’ by Kokko and
Jennions). When females are sexually promiscuous and mate with multiple males (which is more the
rule than the exception in the animal kingdom), these two processes have the potential to continue
also after copulation; intra-sexual selection as sperm competition (Oxford Bibliographies article
*‘Sperm competition’ by Immler) and inter-sexual selection as cryptic female choice. The term ‘cryptic’
is applied since this form of female choice can be hard to observe (e.g. when it occurs inside the
female reproductive tract) and hard to quantify with classical measures of reproductive success (e.g.
mating success). In addition, this form of female choice is hard to disentangle from other episodes of
sexual selection (see below). The framework used to understand female choice occurring after (or
sometimes during) copulation, is currently somewhat divergent, since some authors adopt a very
broad definition of cryptic female choice, while others apply a more conservative definition (see
discussion of this below, under ‘Definition and history’). Cryptic female choice is a relatively young
research topic (it first started properly after Eberhard’s seminal book that was published in 1996). It
was realised early on in the history of the field that a broad range of mechanisms across a variety of
species exist through which females can potentially bias the outcome of a copulation (e.g. ejaculate
ejection, differential sperm storage, sperm choice, see below, ‘Mechanisms and processes used as
cryptic female choice’). As a consequence, measures of pre-copulatory processes or sperm
competition can be misleading in species with cryptic female choice due to also female postcopulatory influences on fertilisation. Yet, although there is no doubt that females have great potential
to bias paternity at the post-copulatory stage, cryptic female choice is the least studied of the
processes through which sexual selection can occur (e.g. compared to sperm competition, or malemale competition). This is probably because demonstration of cryptic female choice is notoriously
difficult. It can be challenging to separate pre- from post-copulatory processes, the interaction of male
adaptations to sperm competition and female influences on fertilisation, and variation in differential
embryo mortality from female-induced biases in paternity (see ‘Potential pitfalls in the study of cryptic
female choice’). The studies that have convincingly been able to separate these processes and
demonstrate cryptic female choice are currently primarily from insect, bird and externally fertilising
species (see ‘Mechanisms and processes used as cryptic female choice’). I here also present some
techniques that can be useful for studies of cryptic female choice, when we may expect to observe
cryptic female choice, how females may benefit from cryptic female choice, and some of the little
theoretical work that includes cryptic female choice.
General overviews
The cryptic female choice field originated during the early 1990’s, with only few papers published
beforehand. Compared to other areas of sexual selection, there are relatively few books or review
articles fully dedicated to cryptic female choice. However, there is one large exception to this, which is
also the book that convincingly established cryptic female choice as an important component of
sexual selection; Eberhard’s seminal book ‘Female control: Sexual selection by cryptic female choice’,
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which was published in 1996. Eberhard presents numerous potential mechanisms by which females
can conduct post-copulatory choice, ranging from female behaviour during copulation through to
female physiology and morphology, to varying investment in offspring. Another important book is
Møller and Birkhead 1998, which gives an excellent overview of post-copulatory sexual selection
across a broad range of taxonomic groups. Although this book focuses on sperm competition, several
chapters are of great relevance for cryptic female choice. Similarly, Birkhead, Pitnick and Hosken
2009 gives an extensive treatment across the broad topic of sperm biology. Several chapters in this
book are also of direct relevance for researchers interested in cryptic female. Additionally, Eberhard
presented a short and updated paper in 2009, which includes a list of a broad range of potential
mechanisms under female control that could bias the outcome of a copulation. Of the relevant journal
articles, Birkhead’s paper in Evolution 1998 (see ‘Potential pitfalls in the study of cryptic female
choice’) and the replies published following it particularly Pitnick and Brown 2000, and Birkhead 2000
(see ‘Potential pitfalls in the study of cryptic female choice’) that discuss how to demonstrate cryptic
female choice, thus are key publications in the field. Due to the many and complex ways ejaculates
and females, and sperm and eggs can interact, Eberhard 1996 and Pitnick et al 2009 (see Definition
and history) suggested that the dichotomy of sperm competition vs. cryptic female choice may not be
very useful, but to instead call the entirety post-copulatory sexual selection. This again highlights that
separating cryptic female choice from other processes can be difficult, in turn making the study of
cryptic female choice hard. A small number of excellent recent review papers summarise
understanding of post-copulatory sexual selection and incorporate cryptic female choice, including
Birkhead and Pizzari 2002, Simmons 2001, 2005 (see ‘Potential pitfalls in the study of cryptic female
choice’), Andersson and Simmons 2006, Birkhead 2010 (see ‘Definition & history’), Parker and
Birkhead 2013 (see ‘Definition & history’). Finally, Birkhead 2000 is a popular science book that
presents scientifically accurate and entertaining examples of post-copulatory sexual selection
(although mainly focusing on sperm competition).
Eberhard WG 1996. Female control: Sexual selection by cryptic female choice . Princeton, NJ:
Princeton University Press.
The seminal monograph demonstrating that cryptic female choice can have important
implications for sexual selection. Eberhard presents an extensive coverage of the many
potential avenues through which females can bias paternity. Eberhard’s book is still the main,
and so far only, book focusing entirely on cryptic female choice.
Birkhead TR & AP Møller 1998. (eds) Sperm competition and sexual selection. Academic Press
London.
A brilliant book reviewing three decades of research on sperm competition in various taxa.
Particularly relevant chapters for cryptic female choice are Parker (see ‘Theoretical models
including cryptic female choice’), Eberhard, Simmons & Siva-Jothy (sperm competition in
insects), Birkhead (sperm competition in birds), and Birkhead and Møller’s concluding chapter
on the various routes through which males and females can affect fitness.
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Birkhead TR 2000. Promiscuity: An evolutionary history of sperm competition . Cambridge, MA:
Harvard University Press.
An entertaining popular science book that presents sperm competition from an evolutionary
perspective accessible to both researchers and the wider public.
Simmons LW 2001. Sperm Competition and its Evolutionary Consequences in the Insects . Princeton:
Princeton University Press.
An extensive review of three decades of research on post-copulatory sexual selection
(including cryptic female choice), in insects. Chapter 9 ‘Ejaculate manipulation: Mechanisms
of female choice’ is particularly relevant for researchers interested in cryptic female choice.
Birkhead TR & T Pizzari 2002. Postcopulatory sexual selection. Nature Reviews: Genetics 3:262–273.
doi: 10.1038/nrg774
This review provides a useful overview of post-copulatory sexual selection, including cryptic
female choice.
Andersson M & LW Simmons 2006. Sexual selection and mate choice. Trends in Ecology and
Evolution 21:296–302. doi: 10.1016/j.tree.2006.03.015
This is a review of studies on mate choice from the prior two decades (both empirical and
theoretical), and also includes mate choice occurring after copulation.
Eberhard WG 2009. Postcopulatory sexual selection: Darwin’s omission and its consequences.
Proceedings of the National Academy of Sciences of the United States of America 106:10025–10032.
doi: 10.1073/pnas.0901217106
This is a more recent summary of Eberhard’s view on post-copulatory sexual selection
including cryptic female choice. The paper includes a table listing a broad range of routes
through which females can potentially bias the outcome of a copulation.
Birkhead TR, DJ Hosken & S Pitnick (eds) 2009. Sperm biology: An evolutionary perspective.
Amsterdam and London: Elsevier/Academic Press.
The most recent and extensive overview of sperm competition and sperm biology. More
relevant chapters with regards to cryptic female choice are Pitnick et al and Karr et al (see
Mechanisms and processes used as cryptic female choice‘), Birkhead and Montgomerie (see
‘Definition and history’).
Journals
Many of the broader scientific journals publish papers on cryptic female choice, such as
**Proceedings of the American naturalist**, **Evolution**, **Journal of Evolutionary Biology**,
**Proceeding of the Royal Society of London B. ** Demonstrations of more behaviourally expressed
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cryptic female choice mechanisms may be published in more behaviourally focused journals, e.g.
**Behavioral Ecology**, Behavioral Ecology and Sociobiology. Because molecular methods are often
used to determine paternity as a measure of fertilisation bias (see discussion on this below), studies
on cryptic female choice using molecular tools may be published in journals such as **Molecular
Ecology**. Reviews on related topics are published in **Trends in Ecology and Evolution**, and
because of its attraction to a broad audience, studies on cryptic female choice can also be published
in leading journals, such as **Science** and **Nature**.
American Naturalist. 1867–.
http://www.press.uchicago.edu/ucp/journals/journal/an.html
Published by the American Society of Naturalists. American Naturalist focuses on conceptual
work often combined with empirical studies in the study of organic evolution and biology in a
broader sense.
Animal Behaviour. 1953-.
http://www.journals.elsevier.com/animal-behaviour/
Published jointly by the UK-based Association for the Study of Animal Behaviour and the USbased Animal Behavior Society. Animal Behaviour publishes papers on advances in the study
of animal behaviour and behavioural ecology.
Behavioral Ecology. 1990- .
http://beheco.oxfordjournals.org/
Published by the International Society of Behavioral Ecology. Behavioral Ecology is a key
journal within the field of behavioural ecology in a broad sense, and focuses generally on
animal behaviour from an evolutionary perspective.
Behavioral Ecology and Sociobiology. 1976- .
http://www.springer.com/life+sciences/behavioural/journal/265/PSE
Published by Springer. Behavioral Ecology and Sociobiology is a key journal within the field of
behavioural ecology in a broad sense, and focuses generally on animal behaviour from both a
proximate and ultimate perspective.
Evolution. 1946-.
http://onlinelibrary.wiley.com/journal/10.1111/%28ISSN%291558-5646
Published by the Society for the Study of Evolution. Evolution is a leading journal in the field
of evolutionary ecology reporting advances in organic evolution, including ecology and
genetics.
Journal of Evolutionary Biology. 1988-.
http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1420-9101
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Published by the European Society for Evolutionary Biology. The journal covers a wide range
of topics in evolutionary biology.
Nature. 1869–.
http://www.nature.com/nature/index.html
Published by Nature Publishing Group. This leading journal in the field of life sciences
publishes research results of broadest general interest.
Molecular Ecology. 1992-.
http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1365-294X
Published by Wiley. Molecular Ecology publishes papers that use molecular methods for
studying ecological and evolutionary questions.
Proceedings of the National Academy of Sciences. 1914-.
http://www.pnas.org/
Published by United States Academy of Science. Ranked below Nature and Science but still
a leading broad interest journal across the sciences, and publishes influential papers in
evolutionary ecology.
Proceedings of the Royal Society of London B: Biological Sciences. 1905-.
http://rspb.royalsocietypublishing.org/
A branch of the Proceedings of the Royal Society of London . The journal publishes articles
that cover a wide range of biological disciplines and is particularly strong in organismal
biology.
Science. 1880–.
http://www.sciencemag.org/
Published by the American Association for the Advances of Science. Next to Nature, Science
is the other leading journal in the field of life sciences.
Trends in Ecology & Evolution. 1986-.
http://www.journals.elsevier.com/trends-in-ecology-and-evolution/
Published by Cell Press. This journal publishes important review and opinion articles at the
forefront of ongoing research in the fields of ecology and evolution.
Definition and history
The seminal paper by Parker1970 demonstrated that sexual selection has the potential to continue
also after copulation. Although Parker’s paper focused on sperm competition, it opened the possibility
that female processes could also continue post-copulation, and that mating success was not equal
with secured fertilisation/paternity. However, it took several decades until female post-copulatory
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processes became an important focus of sexual selection research. Thornhill 1983 refers to earlier
work by Dzierzin 1845, Cohen 1974 and Villavaso 1975 suggesting female control of sperm release
and the female tract to potentially be able to bias sperm use, Birkhead & Møller 1998 refer to work by
Lloyd 1979 suggesting ‘a female choice during or after mating’, and Simmons & Siva-Jothy 1998
gives Sivinsky 1984 the credit for the idea of sperm selection. Nevertheless, Thornhill 1983 (see
‘Mechanisms and processes used as cryptic female choice‘) first used the term cryptic female choice
for female choice occurring ‘during or after mating’. Thornhill & Alcock 1983 described cryptic female
choice as a ‘female imposed paternity bias’. Birkhead & Møller 1993 presented 4 stages through
which females had the potential to bias paternity; before, during, and after copulation (but before
fertilisation), or following fertilisation. In 1996, Eberhard’s landmark monologue on female control of
paternity and potential mechanisms through which cryptic female choice could potentially occur was
published. Eberhard dispatched the idea of passive females in sexual selection, presenting a view
whereby females ‘set the playing field’ and have ‘a finger’ in all ‘games’. Eberhard throughout 1996;
1998; 2009 uses a very broad definition of cryptic female choice: ‘a female controlled process or
structure that selectively favours paternity by conspecific males with a particular trait over that of
others that lack the trait when females has copulated with both types of males’, and he concludes that
cryptic female choice is commonly demonstrated. However, such a broad definition has been
critiqued. Birkhead 1998and the articles published following this, such as Pitnick & Brown 2000,
Birkhead 2000 (see ‘Potential pitfalls in the study of cryptic female choice’), are important
contributions clarifying the specific criteria for demonstrating cryptic female choice to include only
female-driven post-copulatory processes while ruling out e.g. male driven processes. A distinction is
suggested between passive vs. active cryptic female choice along with clarification of sperm choice
vs. cryptic female choice more broadly. As a result of these criteria, cryptic female choice is still
potentially common and important, but has not so often been convincingly, experimentally
demonstrated. Birkhead & Møller’s 1998 and Birkhead et al’s 2009 extensive books review the
research field of post-copulatory sexual selection and show that female influences on paternity can be
substantial. Birkhead 2010 and Birkhead & Parker 2013 have given recent summaries of the history of
post-copulatory sexual selection, including cryptic female choice.
Parker GA 1970. Sperm competition and its evolutionary consequences in the insects. Biological
Reviews 45:525–567. doi: 10.1111/j.1469-185X.1970.tb01176.x.
Parker’s seminal paper founded the field of sperm competition and at the same time
emphasised that sexual selection can continue after copulation. The paper therefore opened
the stage for post-copulatory sexual selection being an important part of sexual selection.
Eberhard WG 1996. Female control: Sexual selection by cryptic female choice . Princeton, NJ:
Princeton University Press.
Eberhard’s extensive overview of cryptic female choice, including a very wide range of
structural, physiological and behavioural traits that can bias fertilisation. Not all of these
potential mechanisms have been experimentally demonstrated to be under female control.
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Eberhard GW 1998. Female roles in sperm competition. In Birkhead TR & AP Møller (eds) Sperm
competition and sexual selection. Academic Press London.
A complement to his monograph (1996). Eberhard makes the point that post-copulatory male
competition and cryptic female choice are not mutually exclusive alternatives, but that the
processes can interplay in complex ways.
Birkhead TR & AP Møller 1998. Sperm competition, sexual selection and different routes to fitness. In
Birkhead TR & AP Møller (eds) Sperm competition and sexual selection. Academic Press London.
This is a review focusing on sperm competition and a summary of the whole book. Three
criteria are presented for detecting cryptic female choice; variation in fertilisation success, and
assignment of this variation to female and male traits.
Pitnick S, MF Wolfner & SS Suarez 2009. Ejaculate-female and sperm-female interactions. In
Birkhead TR, DJ Hosken & S Pitnick (eds) Sperm biology: An evolutionary perspective. Amsterdam
and London: Elsevier/Academic Press.
The complexity of interactions between females and ejaculates/sperm, are reviewed. This
complexity also makes the authors suggest that distinguishing between sperm competition
and cryptic female choice often presents a false dichotomy and they encourage the usage of
‘postcopulatory sexual selection’.
Birkhead TR 2010. How stupid to not have thought of that: post-copulatory sexual selection. Journal
of Zoology 281:78–93. doi:10.1111/j.1469-7998.2010.00701.x.
Birkhead’s historical review gives an overview on how views have changed and progress
made in the history of sexual selection, including the relatively newer understanding that
cryptic female choice can have important evolutionary implications.
Parker GA & TR Birkhead 2013. Polyandry: the history of a revolution. Philosophical Transactions of
the Royal Society of London B 368:20120335.
A recent historical overview of adaptive explanations for polyandry from the female
perspective. The paper uses the history of avian polyandry research as a case example to
demonstrate how views on female sexual promiscuity have changed over time.
Birkhead TR & R Montgomerie 2009. Three centuries of sperm research. In Birkhead TR, DJ Hosken
& S Pitnick (eds) Sperm biology: An evolutionary perspective. Amsterdam and London:
Elsevier/Academic Press.
An excellent historic overview of sperm biology with fantastic images of early drawings of
sperm, and also their interactions with the egg.
When to expect cryptic female choice
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There are several conditions under which cryptic female choice may be more likely to have evolved.
Thornhill 1983 suggest female investment and limitations in ability to assess male quality by
phenotypic trait to be important. Birkhead 1998, Parker & Birkhead 2013 (referred to above) suggest
that when female pre-copulatory mate choice is limited or overridden by males (e.g. due to sexual
harassment or forced copulations; for reviews on sexual conflict see e.g. Arnqvist & Rowe 2005,
Oxford Bibliographies article ‘Sexual conflict’ by Fricke), or if copulatory cues or choice are not
possible for other reasons (e.g. if choice occurs at the level of the gametes, see below Sperm-egg
interactions), females’ potential to conduct post-copulatory mate choice will be favoured in sexual
selection. Female sperm storage, described by Holt 2011 for domesticated animals, described in birds
by King et al 2002 and in insect by for example Simmons 2001, Ward 2007, Pitnick et al 2009, can
separate mating from fertilisation, potentially prolonging the time span during which females can
perform a cryptic choice, and can also be complex which may facilitate female choice.
Thornhill R 1983. Cryptic female choice and its implications in the scorpionfly Harpobittacus nigriceps.
American Naturalist 122:765–88.
Thornhill suggested that post-fertilisation female choice is expected in situations in which
female parental care of zygotes occurs and females can assess the quality of males by
zygotic characteristics to a greater degree than by male phenotypic or gametic traits.
King LM, JP Brillard, WM Garrett, MR Bakst, AM Donoghue 2002. Segregation of spermatozoa within
sperm storage tubules of fowl and turkey hens. Reproduction 123:79-86.
The paper provides information on sperm storage in birds. Inseminations of stained sperm of
female birds indicate that sperm from different inseminations segregate in different sperm
storage tubules.
Simmons LW 2001. Sperm Competition and its Evolutionary Consequences in the Insects . Princeton,
NJ: Princeton University Press.
Simmons argues that insects may be the best group to study post-copulatory sexual selection
in, among other reasons due to the extraordinarily diversity of sperm transfer and storage
mechanisms. The book reviews three decades of post-copulatory sexual selection including
cryptic female choice.
Arnqvist G & L Rowe 2005. Sexual conflict. Princeton, NJ: Princeton University Press.
The most recent and largest review on the topic sexual conflict. The book covers a broad
range of examples and taxa.
Ward PI 2007. Postcopulatory selection in the yellow dung fly Scathophaga stercoraria (L.) and the
mate-now-choose-later mechanism of cryptic female choice. In Advances in the study of behavior.
343–369. San Diego, CA: Elsevier Academic.
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A review of the post-copulatory processes in the well-studied yellow dung fly, including details
on sperm storage and sperm use.
Pitnick S, MF Wolfner & SS Suarez 2009. Ejaculate-female and sperm-female interactions. In
Birkhead TR, DJ Hosken & S Pitnick (eds) Sperm biology: An evolutionary perspective. Amsterdam
and London: Elsevier/Academic Press.
The chapter provides a detailed review of female-ejaculate interactions including female
reproductive tract-induced modification of ejaculates, mainly focusing on insect species.
Holt WV 2011. Mechanisms of sperm storage in the female reproductive tract: an interspecies
comparison. Reproduction in Domesticated Animals. 46:68-74. doi: 10.1111/j.14390531.2011.01862.x.
A review of variation in female sperm storage in various animals.
Potential pitfalls in the study of cryptic female choice
Many authors highlight the observation that it can be hard to disentangle cryptic female choice from
other processes influencing the measure used to investigate cryptic female choice. Thornhill 1983
points out that separation of male and female driven processes can be nontrivial. Birkhead 1998,
2000 and Møller 1998 and Birkhead et al 2009, Pitnick & Brown 2000, among others, also make this
point together with highlighting that it can be difficult to disentangle a post-copulatory bias from a precopulatory bias. Eberhard 1996 and Pitnick et al 2009 suggest that the dichotomy of cryptic female
choice and sperm competition may be better be called post-copulatory sexual selection due to the
complex interactions between the sexes. For studies that use paternity measures to estimate potential
biases in which males’ sperm a female uses, Birkhead 1998, Olsson et al 1999 and Simmons 2005
emphasis that differential embryo mortality can also be a confounding effect that should be
considered. Simmons 2006 highlights that maternal effects also can bias measures of cryptic female
choice. Simmons et al 2006 and Evans et al 2013 present studies exemplifying the potential
complexity of processes that can affect measures of cryptic female choice.
Thornhill R 1983. Cryptic female choice and its implications in the scorpionfly Harpobittacus nigriceps.
American Naturalist 122:765–88.
Thornhill highlights that a problem in studies of sexual selection has been the difficulty of
separating male-male competition from female choice as agents causing differential success
of males.
Birkhead TR 1998. Cryptic female choice: criteria for establishing female sperm choice. Evolution
52:1212-1218.
Birkhead encourages a more rigorous approach to demonstrating cryptic female choice than
previously employed, including the importance of controlling for male-mediated effects and
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differential abortion. Birkhead concludes that current studies that have done so are rare. The
paper generates valuable discussion on the topic (see ‘Definition and History’).
Pitnick S & W Brown 2000. Criteria for demonstrating female sperm choice. Evolution 54:1052-1056.
Pitnick and Brown’s reply to (Birkhead 1998) where the authors suggest an improved method
and a slightly modified definition of cryptic female choice: ‘nonrandom paternity biases
resulting from female morphology, physiology or behaviour that occur after coupling’. They
actively avoid ‘control’ allowing also more passive female-explained biases to be included.
Birkhead TR 2000. Defining and demonstrating postcopulatory female choice –again. Evolution
54:1057-1060.
This is Birkhead’s reply to the papers following his initial paper on how to define and
demonstrate cryptic female choice (Birkhead 1998). The paper presents a modified definition
and protocol to be used to demonstrate cryptic female choice, and makes the distinction
between ‘active’ and ‘passive’ cryptic female choice.
Olsson M, M Pagel, R Shine, T Madsen, C Doums, A Gullberg & H Tegelström 1999. Sperm choice
and sperm competition: suggestions for field ad laboratory studies. Oikos 84:172-175.
The authors urge that differential embryo mortality needs to be ruled out as a confounding
effect, particularly for studies on cryptic female choice and hybridisation, inbreeding
avoidance or investigating effects of differences in the Major Histocompatibility Complex
(MHC) among partners.
Simmons L 2005. The evolution of polyandry: Sperm competition, sperm selection and offspring
viability. Annual Reviews in Ecology Evolution Systematics 36:125-146.
Simmons presents a review and meta-analyses of female benefits of polyandry, focusing on
genetic benefits. Simmons highlights that maternal effects need to be controlled because of
its potential bias of paternity patterns between genetically incompatible partners.
Simmons LW, P Stockley, RL Jackson & GA Parker 2006. Sperm competition or sperm selection: No
evidence for female influence over paternity in yellow dung flies Scatophaga stercoraira. Behavioral
Ecology and Sociobiology 38:199-206.
An example on how in practise it can be very hard to disentangle male and female factors in
the utilisation of sperm.
Evans JP, P Rosengrave, C Gasparini & NJ Gemmell 2013. Delineating the roles of males and
females in sperm competition. Proceedings of the Royal Society of London B 280:20132047. doi:
10.1098/rspb.2013.2047.
This paper aims to disentangle the relative roles of males and females in fertilisation bias
through an ambitious series of factorial crosses.
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Some useful techniques
A careful experimental design is typically needed to be able to demonstrate cryptic female choice. In
addition, several techniques can be used aiming to tease apart female driven processes from other
processes that may affect sperm storage/paternity. Birkhead et al 2004 and Løvlie et al 2013
demonstrate how artificial insemination can be used to control number of sperm inseminated and
remove pre-copulatory cues, Manier et al 2010 show how colour labelling of sperm and observation of
their behaviour inside the female can be used to further out understanding of post-copulatory
processes, Løvlie et al 2013 is an example of how counting the sperm reaching the perivitelline layer
of eggs in birds can provide information on female sperm use, and Bretman et al 2009 is an example
of who genotyping of sperm in the female sperm storage organs enables cryptic female choice to be
inferred.
Artificial insemination
Birkhead 2000 (references to above) suggests the use of artificial insemination to uncouple male
phenotypic trait and ejaculate/sperm trait. Through the use of artificial insemination, Birkhead et al
2004 demonstrated cryptic female choice owing to genetic compatibility between different breeds of
domestic fowl. In red junglefowl, Løvlie et al 2013 detected cryptic female choice in favour of
genetically dissimilar males following natural copulations, but not after artificial insemination. Other
studies, such as Denk et al 2005, have also failed to observe cryptic female choice following artificial
insemination. This adds a cautionary note on the use of artificial insemination as a technique to
determine cryptic female choice, and more work on the functional significance of insemination method
and cryptic female choice may therefore be needed.
Birkhead TR, Chaline N, Biggins JDT, Burke T & T Pizzari 2004. Nontransivity of paternity in a bird.
Evolution 58:416–420.
The authors mixed equal numbers of sperm from two males and artificially inseminated the
sperm into females, demonstrating that male-female interactions affect paternity.
Denk AG, Holzmann A, Peters A, Vermeirssen ELM & B Kempenaers 2005. Paternity in mallards:
effects of sperm quality and female sperm selection for inbreeding avoidance. Behavioral Ecology
16:825–833. doi:10.1093/beheco/ari065.
The authors inseminated female ducks artificially controlling for sperm traits, but failed to find
a post-copulatory female bias in sperm use against related males.
Løvlie H, MAF Gillingham, K Worley, T Pizzari & DS Richardson 2013. Cryptic female choice favours
sperm from major histocompatibility complex-dissimilar males. Proceedings of the Royal Society of
London B. 280: 20131296. dx.doi.org/10.1098/rspb.2013.1296.
In natural copulations, female red junglefowl favours the sperm of males that are MHCdissimilar to the female. This pattern was not detected when ejaculates were inseminated
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artificially. Both pre-copulatory mate choice, female ejaculate ejection, male differential sperm
allocation and embryo mortality are controlled for.
Florescent protein labelling of sperm prior to insemination
Beautiful work by Manier et al 2010 demonstrates that by labelling sperm, the interaction between
different males’ sperm, and also their interaction with the female, can be facilitated.
Manier MK, JM Belote, KS Berben, D Novikov, WT Stuart, & S Pitnick 2010. Resolving mechanisms
of competitive fertilization success in Drosophila melanogaster. Science 328:354–357. doi:
10.1126/science.1187096.
The authors labelled sperm of male flies using different florescent colours. The technique
enabled live observations of the interactions of sperm of different males, and also their
interaction with the female reproductive tract.
Counting sperm in female storage organs
By knowing the number of sperm inseminated, counting the number of sperm a female store can give
information on biases in processes occurring up to and during sperm storage. The technique of
counting the number of sperm stored by a female has been described for example for fish by Pilastro
et al 2002, insects by Fedina 2007 and spiders by Albo et al 2013 (see Copulation courtship).
Pilastro A, Evans J P, Sartorelli S & A Bisazza 2002. Male phenotype predicts insemination success
in guppies. Proceedings of the Royal Society of London B 269:1325-1330.
doi:10.1098/rspb.2002.2017.
Quickly after insemination, the gonoducts of anaesthetized female guppies were flushed with
known amount of solution, further enabling the number of sperm obtained from each female
to be counted.
Fedina TY 2007. Cryptic female choice during spermatophore transfer in Tribolium castaneum
(Coleoptera: Tenebrionidae). Journal of Insect Physiology. 53:93-97.
doi:10.1016/j.jinsphys.2006.10.011.
Female flour beetles were killed after copulation and their reproductive tract dissected
enabling size of spermatophore and sperm number stored, to be counted.
Genotyping of sperm in female storage organs
By genotyping the sperm collected from the female sperm storage organs, the proportion of sperm
from different males stored by the female can be estimated. This has been demonstrated in crickets,
by Bretman et al 2009.
Bretman A, Newcombe D & T Tregenza 2009. Promiscuous females avoid inbreeding by controlling
sperm storage. Molecular Ecology 18:3340-3345. doi: 10.1111/j.1365-294X.2009.04301.x.
13
A competitive microsatellite polymerase chain reaction technique (CM-PCAR) was used to genotyped
sperm in spermatecha of female field crickets. The number of sperm stored was biased in favour of
unrelated males, a pattern not explained by pre-copulatory bias or male differential sperm allocation.
Counting the number of hydrolysis points on the perivitelline layer of eggs
In birds, Wishart 1987 describes how the number of hydrolysis points on the outer perivitelline layer
(PVL) of the yolk caused by individual live sperm cells around the time of fertilization can be
measured after the egg is laid. This non-invasive technique measures the number of sperm a female
store and use after insemination, but prior to any later biases, for example by embryo mortality. The
technique was used by Løvlie et al 2013 demonstrating cryptic female choice in the red junglefowl.
Wishart GJ 1987. Regulation of the length of the fertile period in the domestic fowl by numbers of
oviducal spermatozoa, as reflected by those trapped in laid eggs. Journal of Reproduction and
Fertility 80:493–498. doi: 10.1530/jrf.0.0800493.
The paper describes the technique of counting hydrolysis points made by sperm on the
perivitelline layer of eggs laid by females after insemination as a measure of estimating the
number of sperm stored and surrounding the egg in the infundibulum at the time of
fertilisation.
Løvlie H, MAF Gillingham, K Worley, T Pizzari & DS Richardson 2013. Cryptic female choice favours
sperm from major histocompatibility complex-dissimilar males. Proceedings of the Royal Society of
London B 280:20131296. doi: 10.1098/rspb.2013.1296.
Through the use of the PVL-technique, the authors showed that female red junglefowl
discriminated against sperm of males that were more genetically similar to the females
investigated.
Female benefits from cryptic female choice
Similarly as for pre-copulatory mate choice (Oxford Bibliographies article ‘Mate choice’ by Jennions &
Kokko), female benefits of polyandry can be direct (i.e. when females benefit directly, for example
through obtaining nutrients from spermatophores) or indirect (when female benefits indirectly in terms
of improved offspring quality). There are several good reviews on the genetic benefits of polyandry
and how postcopulatory sexual selection can improve offspring quality, provided by for example
Jennions & Petrie 2000, Tregenza & Wedell 2000, Neff & Pitcher 2005, and Simmons 2005 (reviewed
under ‘Potential pitfalls in the study of cryptic female choice’) . Indirect benefits can be explained by
additive genetic benefits and the production of more viable or more attractive offspring. Alternatively,
females can gain non-additive benefits through preference for compatible genomes where
incompatibility can reduce fitness (e.g. through hybridization, inbreeding). Female choice for can in
principle be selection for ‘good sperm’, ‘sexy sperm’, or ‘compatible sperm’ (see below).
14
Jennions MD & M Petrie 2000. Why do females mate multiply? A review of the genetic benefits.
Biological Reviews Cambridge Philosophical Society 75:21-64.
A review of genetic benefits of polyandry and female mate choice, both before and after
copulation.
Neff BD & TE Pitcher 2005. Genetic quality and sexual selection: an integrated framework for good
genes and compatible genes. Molecular Ecology 14:19–38. doi:10.1111/j.1365-294X.2004.02395.x.
An extensive review of genetic benefits of female pre- and post-copulatory choice. An
integrated framework is presented on the terminology of genetic benefits.
Tregenza T & N Wedell 2000. Genetic compatibility, mate choice and patterns of parentage.
Molecular Ecology 9:1013–27.
This is an extensive review presenting studies on both pre- and post-copulatory mate choice
favouring genetic compatibility among partners.
Direct benefits
Rodrigez-Enriquez et al 2013 offers an example of how females may gain direct benefits from their
cryptic female choice.
Rodrigez-Enriquez CL, E Tadeo & J Rull 2013. Elucidating the function of ejaculate expulsion and
consumption after copulation by female Euxesta bilimei. Behavioural Ecology and Sociobiology
67:937-946. doi:10.1007/s00265-013-1518-5.
Females sometimes eject ejaculates after copulation and may also eat this. The study tested
under what conditions females benefitted from doing so, and show that only when starved did
females seem to benefit from eating expulsed ejaculates.
Indirect benefits
Females may gain indirect benefits from their cryptic female choice, from choosing ‘good sperm’, as
suggested by Birkhead et al 1993, and Yashui 1997, ‘sexy sperm’, as suggested by Birkhead et al
1993, and Keller & Reeve 1995 or ‘compatible sperm’, as suggested by Zeh & Zeh 1997, and
reviewed by Zeh & Zeh 2003.
Good sperm
Yasui 1997 presents a ‘good sperm’ hypothesis which posits that high-quality males are better sperm
competitors and sire higher-quality offspring. Simmons & Kotiaho 2002 provide an example of sperm
traits and male quality to be related, and Hosken et al 2003 an example of sperm trait and offspring
quality to be related.
Yasui Y 1997. A “good-sperm” model can explain the evolution of costly multiple mating by females.
American Naturalist 149:573–584. doi: 10.1086/286006.
15
The paper develops an interesting hypothesis about how females may select the best male to
sire offspring by inducing sperm competition. It is based on the assumption that sperm quality
reflects male quality.
Simmons LW & JS Kotiaho 2002. Evolution of ejaculates: patterns of phenotypic and genotypic
variation and condition dependence in sperm competition traits. Evolution 56:1622–1631.
The authors show condition dependence of ejaculate characteristics in the dung beetle
(Onthophagus taurus).
Hosken DJ, TWJ Garner, T Tregenza, N Wedell & PI Ward 2003. Superior sperm competitors sire
high-quality young. Proceedings of the Royal Society of London B 270:1933-1938. doi:
10.1098/rspb.2003.2443.
Male yellow dung flies (Scathophaga stercoraria) that were more successful in sperm
competition produced sons that developed faster, supporting the good sperm hypothesis.
Sexy sperm
Birkhead et al 1993 presents examples of how the female tract may select for better or sexier sperm.
Keller & Reeve 1995 presents the ‘sexy-sperm’ hypothesis which proposes that by creating a
competitive fertilisation environment and sperm competition, females produce sons that are also
successful in sperm competition. Simmons 2003 did not find support for this in crickets.
Birkhead TR, AP Møller & WJ Sutherland 1993. Why do females make it so difficult for males to
fertilize eggs? Journal of Theoretical Biology 161:51–60. doi: 10.1006/jtbi.1993.1039
The paper raises the questions of whether females can use the hostile nature of their
reproductive tract to select sperm and select for better or sexier sperm. Female anti-sperm
responses are discussed.
Keller L & HK Reeve 1995. Why do females mate with multiple males: The sexually selected sperm
hypothesis. Advances in the Study of Behavior 24:291–315. doi: 10.1016/S0065-3454(08)60397-6.
The authors formulate the idea that females select for the best male to sire here offspring by
inducing sperm competition.
Simmons LW 2003. The evolution of polyandry: patterns of genotypic variation in female mating
frequency, male fertilization success and a test of the sexy-sperm hypothesis. Journal of Evolutionary
Biology 16:624–34.
Patterns of fertilisation success of male field crickets (Telegryllus oceanicus) do not support
the sexy-sperm hypothesis.
Compatible sperm
16
Females may also choose the male or sperm to fertilise her eggs that is the best genotypic match, i.e.
that the best sperm are those bearing haplotypes most compatible with the female genome or that
minimize genetic incompatibility. Some of the strongest evidence in favour of the genetic compatibility
hypothesis comes from experiments on inbreeding avoidance, as demonstrated in insects by
Tregenza & Wedell 2002 and Bretman et al 2009 (reviewed above, ‘Some useful techniques’), and in
lizards by Olsson et al 1996, and dissimilarity in MHC, as demonstrated in rodents by Wedekind et al
1996, in fish by Yeates et al 2009, and in birds by Løvlie et al 2013 (reviewed above, ‘Some useful
techniques’). The general importance of genetic compatibility in post-copulatory sexual selection is
reviewed for example by Zeh & Zeh 1997, 2003, Tregenza and Wedell 2000 and Simmons 2005
(reviewed above, ‘Potential pitfalls in the study of cryptic female choice’), and for example Bjork et al
2007 (reviewed under Female reproductive tract-ejaculate interactions), Birkhead et al 2004
(reviewed under Artificial insemination), and Bilde et al 2008 show that male-female interactions affect
fertilisation success, paternity and offspring productivity, respectively.
Wedekind C, Chapuisat M, Macas E & T Rülicke 1996. Non-random fertilization in mice correlates
with the MHC and something else. Heredity 77:400–409. doi: 10.1038/hdy.1996.160.
In mice (Mus musculus), nonrandom fertilization with bias towards MHC heterozygosity was
observed, likely mediated by sperm–egg interactions.
Olsson M, Shine R, Madsen T, Gullberg A & H Tegelström 1996. Sperm selection by females. Nature
383:585.
In sand lizards (Lacerta agilis), fertilization success of polyandrous females was greater for
sperm from males genetically dissimilar to the female.
Zeh JA & Zeh DW 1997. The evolution of polyandry II: post-copulatory defences against genetic
incompatibility. Proceedings of the Royal Society London B 264:69–75.
The importance of genetic compatibility among partners in post-copulatory sexual selection
came to prominence via Zeh & Zeh’s work. This paper reviews how post-copulatory sexual
selection can enable polyandrous females to minimize the risk of fertilization by genetically
incompatible sperm.
Zeh JA & DW Zeh 2003. Toward a new sexual selection paradigm: Polyandry, conflict and
incompatibility. Ethology 109:929–950. doi: 10.1046/j.1439-0310.2003.00945.x.
A review summarising the idea that female polyandry is a strategy for females to ensure
fertilisation by genetically compatible males through mechanisms taking place between
sperm-egg and/or sperm-female reproductive tract interactions.
Tregenza T & N Wedell 2002. Polyandrous females avoid costs of inbreeding. Nature 415:71–73.
17
Females mated to one full sibling and one unrelated male had the same hatching success as
those that had mated with two unrelated males, suggesting that sperm from unrelated males
were used preferentially rescuing a bias against related males’ sperm.
Yeates SE, S Einum, IA Fleming et al 2009. Atlantic salmon eggs favour sperm in competition that
have similar major histocompatibility alleles. Proceedings of the Royal Society of London B 276:559–
566. doi: 10.1098/rspb.2008.1257
Fertilisations carried out in vitro show that eggs are fertilized by sperm from males with more
dissimilar MHC, demonstrating cryptic female choice at the sperm-egg level for compatible
sperm.
Bilde T, U Friberg, A Maklakov, J D Fry & G Arnqvist 2008. The genetic architecture of fitness in a
seed beetle: assessing the potential for indirect genetic benefits of female choice. BMC Evolutionary
Biology 8:295. doi:10.1186/1471-2148-8-295.
In seed beetles, both additive and non-additive effects affected offspring production, where
male-female interaction effects were more pronounced.
Mechanisms and processes used as cryptic female choice
Whether the definition applied is broad or more narrow, there are a range of behavioural,
physiological, chemical, morphological and genetic processes through which females can potentially
bias paternity. Birkhead & Møller 1993, and Eberhard’s extensive monolog 1996 and his later papers
review these (e.g. Eberhard 2009). Simmons 2001, and several chapters in Birkhead and Møller
1998, and Birkhead et al 2009, such as Pitnick et al 2009, also present various means of cryptic
female choice (see above for relevant chapters). In addition, Birkhead & Brillard 2007 is a good
review of the various stages in the female reproductive tract where biases can occur, of particularly
relevance for avian species. Here I present examples to show some of the breath of potential
mechanisms, and in the range of taxa, through which cryptic female choice has been investigated so
far.
Birkhead TR & AP Møller 1993. Female control of paternity. Trends in Ecology and Evolution. 8:100104.
The review gives an overview of the stages of the breeding cycle that female paternity control
may occur. The authors provide a figure of the dramatic drop in sperm numbers ejaculated
and towards the site of fertilisation.
Birkhead TR & J-P Brillard 2007. Reproductive isolation in birds: postcopulatory prezygotic barriers.
Trends in Ecology and Evolution. 22:266-272. doi:10.1016/j.tree.2007.02.004.
A review of studies of interspecific hybridization in domesticated birds. The analyses of
studies so far strongly suggest that immunological sperm–female recognition is involved in
bias of paternity.
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Eberhard WG 2009. Postcopulatory sexual selection: Darwin’s omission and its consequences.
Proceedings of the National Academy of Sciences of the United States of America 106:10025–10032.
doi: 10.1073/pnas.0901217106
Eberhard reviews previous work and presents a broad list of routes through which females
can bias the outcome of a copulation.
Pitnick S, MF Wolfner & SS Suarez 2009. Ejaculate-female and sperm-female interactions. In
Birkhead TR, DJ Hosken & S Pitnick (eds) Sperm biology: An evolutionary perspective. Amsterdam
and London: Elsevier/Academic Press.
The authors list the conditions that exist before sperm can fertilise an egg, including physical
and chemical barriers, and a summary of the dramatic drop in numbers of sperm inseminated
vs the number of sperm reaching the site of fertilisation.
Copulation courtship
Male behaviour during copulation can affect female sperm use/bias paternity in favour of certain
males, as suggested by several authors such as Eberhard 1996,Otronen & Siva-Jothy 1991,
Edvardsson & Arnqvist 2000. This type of influence on paternity highlights the intertangled nature of
male and female interactions affecting the outcome of a mating and demonstrates how hard it can be
to disentangle male and female influences on post-copulatory sexual selection. Eberhard 1996 (see
‘General overview’) refers to this phenomenon as cryptic female choice. However, whether females
can use this in an active way under female control has still not been shown.
Otronen M & MT Siva-Jothy 1991. The effect of postcopulatory male behaviour on ejaculate
distribution within the female sperm storage organ of the fly, Dryomyza anilis (Diptera: Dryomyzidae).
Behavioral Ecology 5:51-56.
Females respond to male tapping during copulation by releasing stored sperm.
Edvardsson M & G Arnqvist 2000. Copulatory courtship and cryptic female choice in red flour beetles
Tribolium castaneum. Proceedings of the Royal Society of London B 267:559-563.
The authors experimentally manipulate male copulatory courtship behaviour, showing that
female perception rather than male behaviour per se affect male fertilisation success.
Albo M, Bilde T & G Uhl 2013. Sperm storage mediated by cryptic female choice for nuptial gifts.
Proceedings of the Royal Society of London B 280:20131735. doi:10.1098/rspb.2013.1735.
Female spiders mated to males allowed to offer a nuptial gift had more sperm stored
(investigated by counting number of sperm in their spermathecae after mating), compared to
females mated to males that did not offer a gift. Copulation duration, which is suggested to be
under female control, correlates with number of sperm counted in females’ spermathecae.
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Female control of oviposition
Female speed of oviposition was the initial process by which Thornhill 1983 investigated female
influence on paternity. Whether a female initiates oviposition directly after a mating or delays it until
she has re-mated, can bias who fathers her eggs. This is a potentially widespread mechanism of
cryptic female choice, as discussed by Eberhard 1996, however it can be hard to separate from maledriven processes. Barbosa 2009 provides an example where oviposition timing is studied as a
suggested cryptic female choice mechanism.
Thornhill R 1983. Cryptic female choice and its implications in the scorpionfly Harpobittacus nigriceps.
American Naturalist 122:765–88.
Thornhill’s paper is used as the classic reference for cryptic female choice. Thornhill
discusses female choice to occur before, during or after mating. Thornhill makes the
important conclusion that female choice can be cryptic (i.e. hard to measure).
Barbosa F 2009. Cryptic female choice by female control of oviposition timing in a soldier fly.
Behavioral Ecology 20:957–960. doi: 10.1093/beheco/arp083.
The study exposed females to males prevented from courting the females, which resulted in
that females delayed oviposition, which in turn reduces these males’ chances of fertilising the
females’ eggs.
Female reproductive tract morphology
Variation in female reproductive tract morphology (e.g. spermathecha size) can cause a bias in
paternity that is best explained by female variation. Simmons 2001 provide extensive information on
post-copulatory sexual selection in insects, including variation in female tract morphology. Whether
females can use this to actively bias sperm use, however, has not yet been demonstrated.
Simmons LW 2001. Sperm Competition and its Evolutionary Consequences in the Insects . Princeton:
Princeton University Press.
Simmons argues that insects may be the best group to study post-copulatory sexual selection
because of the extraordinarily diversity of sperm transfer and storage mechanism observed.
The book is an extensive review of post-copulatory sexual selection in insect.
Female removal of spermatophore or copulatory plug
Females of various species have been shown to remove the male inseminated spermatophore or
copulation plug after insemination. Eberhard 1996 presents a table on female spermatophore removal
in various species, such as crickets, studied by Simmons 1986, in mammals, studied by Koprowski
1992, and in squid, studied by Sato et al 2013.
Simmons LW 1986. Female choice in the field cricket, Gryllus bimaculatus (De Geer). Animal
Behaviour 34:1463–1470.
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Female crickets can remove, and sometimes also eat, the spermatophore after copulation.
Koprowski JL 1992. Removal of copulatory plugs by female tree squirrels. Journal of Mammalogy
73:572-576.
Females can remove copulatory plugs placed by males post-insemination, after copulation.
Females either discard or consume the plug.
Sato N, Kasugai T & H Munehara 2013. Sperm transfer or spermatangia removal: post copulatory
behaviour of picking up spermatangium by female Japanese pygmy squid. Marine Biology 160:553–
561.
Female pygmy squid can remove spermatangia (capsules containing sperm) after copulation.
Female ejaculate ejection or sperm dumping
A mechanism that can occur during, or direct after copulation, is female differential ejaculate ejection
after insemination. Female ejaculate ejection has been observed in several taxa, such as in
mammals, studied by Ginsberg & Rubenstein 1990, in birds studied by, Pizzari & Birkhead 2000,
Helfenstein et al 2003, and Dean et al 2011, in insects as studied by Snook & Hosken 2004, and
Cordoba-Aguilar 2006. However, Davies 1983 demonstrated that female ejaculate ejection can
sometimes be under male control, thus to demonstrate this to be a female driven bias, male effects
must be controlled for.
Davies NB 1983. Polyandry, cloaca-pecking and sperm competition in dunnocks. Nature 302:334–
336.
Male dunnocks can make females eject stored sperm by gently pecking on their cloaca.
Ginsberg JR & DI Rubenstein 1990. Sperm competition and variation in zebra mating behavior.
Behavioral Ecology and Sociobiology 26:427–434.
The paper compares mating behaviour of two closely related zebra species that vary in their
mating system, including female ejection of ejaculate after copulation.
Pizzari T & TR Birkhead 2000. Female feral fowl eject sperm of subdominant males. Nature 405:787–
789. doi: 10.1038/35015558.
Female fowl are more likely to eject an ejaculate after insemination by a non-preferred
subdominant male, compared to dominant males.
Helfenstein F, RH Wagner & E Danchin 2003. Sexual conflict over sperm ejection in monogamous
pairs of kittiwakes Rissa tridactyla. Behavioral Ecology and Sociobiology 54:370-376. doi:
10.1007/s00265-003-0636-x.
Female kittiwakes can eject ejaculates after copulation which can generate sexual conflict
over sperm use.
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Snook RR & SJ Hosken 2004. Sperm death and dumping in Drosophila. Nature 428:939-941.
Female drosophila can dump sperm in response to copulation, which can explain patterns of
sperm precedence without invoking sperm displacement, incapacitation, or effects of seminal
fluid killing rival sperm.
Cordoba-Aguilar A 2006. Sperm ejection as a possible cryptic female choice mechanism in Odonata
(Insecta). Physiological Entomology 31:146-153. doi: 10.1111/j.1365-3032.2005.00498.x.
The study suggests that female Odonata can bias sperm storage by ejecting sperm.
Dean R, Nakagawa S & T Pizzari 2011. The risk and intensity of sperm ejection in female birds.
American Naturalist 178:343-354.
The authors describe variation in the probability and extent of female ejection of ejaculates in
female fowl. Variation is explained by male social status and female mating history.
Female control of sperm storage
Female bias of the transport of sperm to and from sperm storage organs can affect female sperm use
and bias paternity. Bretman et al 2009, and Tuni et al 2013 demonstrated that this bias can be
affected by relatedness between partners. In spiders, Albo et al 2013 show that copulation duration
affect number of sperm stored by the female, and copulation duration appear to be under female
control (see Copulation courtship).
Bretman A, Newcombe D & T Tregenza 2009. Promiscuous females avoid inbreeding by controlling
sperm storage Molecular Ecology 18:3340-3345. doi: 10.1111/j.1365-294X.2009.04301.x.
Proportion of sperm in spermatecha of females mated by related and unrelated males was
biased in favour of unrelated males. The pattern was not due to male differential sperm
allocation.
Tuni C, Beveridge M & LW Simmons 2013. Female crickets assess relatedness during mate guarding
and bias storage of sperm towards unrelated males. Journal of Evolutionary Biology 26:1261-1268.
doi: 10.1111/jeb.12118.
The authors demonstrate that female bias sperm storage according to the courting male (and
not according to the relatedness of the male the sperm came from).
Female reproductive tract-ejaculate interactions
Cohen & McNaughton 1974, Bishop et al 1996, and Birkhead et al 1993 describes how the female
reproductive tract can be a hostile environment for sperm,Holt & Fazeli 2010 describes how
ejaculates in turn can affect the female tract, and several authors, for example Eberhard 1996,
Birkhead & Møller 1998, Bjork et al 2007, and Pitnick et al 2009 highlight that the interplay between
22
female and ejaculate can be complex and have important influences on fertilisation success or
paternity.
Cohen J & DC McNaughton 1974. Spermatozoa: The probable selection of a small population by the
genital tract of the female rabbit. Journal of Reproduction and Fertility 39: 297-310.
Cohen’s work stresses the role of the female, and show that spermatozoa retrieved from high
in the female tract were found to be better at fertilising eggs, compared to sperm retrieved
further down in the female tract.
Birkhead TR, AP Møller & WJ Sutherland 1993. Why do females make it so difficult for males to
fertilize their eggs? Journal of Theoretical Biology 161:51-60. doi: 10.1006/jtbi.1993.1039.
The authors review the hostility of the female tract to sperm and female anti-sperm
responses, and discuss potential adaptive explanations for this hostility.
Bishop JDD, Jones CS & LR Noble 1996. Female control of paternity in the internally fertilizing
compound ascidian Diplosoma listerianum. II. Investigation of male mating success using RAPD
markers. Proceedings of the Royal Society London B 263:401–7.
In the hermaphroditic ascidian (Diplosoma listerianum) phagocytose of self-sperm in the
oviduct results in a fertilization advantage for genetically dissimilar sperm.
Bjork A, Starmer WT, Higginson DM, Rhodes CJ & S Pitnick 2007. Complex interactions with females
and rival males limit the evolution of sperm offense and defence. Proceedings of the Royal Society of
London B 274:1779–1788.
The paper shows male by male by female effects on fertilisation success. The pattern of
sperm precedence was statistically repeatable only when each male competed against the
same rival male and within the same female.
Pitnick S, MF Wolfner & SS Suarez 2009. Ejaculate-female and sperm-female interactions. In
Birkhead TR, DJ Hosken & S Pitnick (eds) Sperm biology: An evolutionary perspective. Amsterdam
and London: Elsevier/Academic Press.
The chapter of Birkhead & Møller’s book gives a detailed overview of the many and often
complex ways ejaculates and females can interact and affect the paternity of offspring.
Holt WV & A Fazeli 2010. The oviduct as a complex mediator of mammalian sperm function and
selection. Molecular Reproduction and Development 77:934-943.
The paper reviews ejaculate-oviduct interactions in mammals, including up- and downregulation of gene expression in the oviduct on the arrival of sperm.
Ovarian fluid differentially affecting sperm
23
Ovarian fluid can affect sperm in ways biasing paternity, for example by increasing sperm velocity.
This has been demonstrated in fish by Urbach et al 2005 and Gasparini & Pilastro 2011.
Urbach D, I Folstad & G Rudolfsen 2005. Effects of ovarian fluid on sperm velocity in Arctic charr
(Salvelinus alpinus). Behavioral Ecology and Sociobiology 57.5: 438–444. doi: 10.1007/s00265-0040876-4.
Sperm swimming velocity in Arctic charr is differently affected by ovarian fluid of various
females.
Gasparini C & A Pilastro 2011. Cryptic female preference for genetically unrelated males is mediated
by ovarian fluid in the guppy. Proceedings of the Royal Society London B 278: 2495-2501. doi:
10.1098/rspb.2010.2369.
Artificially inseminated females with equal sperm numbers from related and unrelated males
show that ovarian fluid from sisters reduced the velocity of brother’s sperm. The authors
controlled for differential embryo mortality.
Sperm-egg interactions
Vacquier 1998, Palumbi 1999, and Karr et al 2009 have shown that compatibility among gametes can
affect fertilisation efficiency. In external fertilisers, gamete interaction can be the only way females
may be able to carry out a cryptic choice and control fertilisation. Evans & Marshall 2005 and Yeates
et al 2009 have shown sperm-egg interactions to affect fertilisation in fish. Sperm-egg interactions
have also been demonstrated in internally fertilising species, for example in rodents shown by Ronald
& Gomendio 2007, and Friman & Simmons 2013.
Vacquier VD 1998. Evolution of gamete recognition proteins. Science 281:1995–98.
A review of sperm–egg interactions in externally fertilizing species and the importance of
gamete recognition in broadcast spawning animals.
Palumbi SR 1999. All males are not created equal: fertility differences depend on gamete recognition
polymorphisms in sea urchins. Proceedings of the National Academy of USA 96:12632–12637.
Compatibility of the gametes bindin genotype affects fertilisation in the urchin Echinometra
mathaei where eggs selectively fuse with sperm that share the largest number of bindin
alleles.
Evans JP & DJ Marshall 2005. Male-by-female interactions influence fertilization success and mediate
the benefits of polyandry in the sea urchin Heliocidaris erythrogamma. Evolution 59:106-112.
In the Australian urchin Heliocidaris erythrogramma, the proportion of eggs fertilized in
artificial spawning trials was affected by the interaction between male and female genotypes.
Ronald ERS & M Gomendio 2007. Spermatology. Nothingham University press, Nothingham.
24
The edited book ‘Spermatology’ reviews a large number of topics related to sperm function
and fertilisation. Particularly the chapters under the heading ‘Sperm-egg interaction’ are of
relevance for studies on cryptic female choice.
Yeates SE, S Einum, IA Fleming et al 2009. Atlantic salmon eggs favour sperm in competition that
have similar major histocompatibility alleles. Proceedings of the Royal Society of London B 276: 559–
566. doi: 10.1098/rspb.2008.1257.
Fertilisations carried out in vitro show that eggs are fertilized by sperm from males more
dissimilar at the MHC, demonstrating cryptic female choice at the sperm-egg level for
compatible sperm.
Karr TL, WJ Swanson & RR Snook 2009. The evolutionary significance of variation in sperm-egg
interactions. In Birkhead TR, DJ Hosken & S Pitnick (eds) Sperm biology: An evolutionary
perspective. Amsterdam and London: Elsevier/Academic Press.
A thorough review and presentation of the different stages and ways in which sperm and eggs
can interact.
Friman RC & LW Simmons 2013. Sperm competition risk generates phenotypic plasticity in ovum
fertilizability. Proceedings of the Royal Society of London B 280:20132097. doi:
10.1098/rspb.2013.2097.
The study shows that female gametes can adjust fertilisability and resistance to fertilisation
dependent both by the historical sperm competition level of the population, and the level of
sperm competition females faced during development.
Post-insemination pre-fertilisation female bias
A choice can in some cases also occur after insemination, before the pronucleus of males and
females have fused. This has very clearly been observed by Carre & Sardet 1984, and is also
discussed by Goerlick et al 2011.
Gorelick R, LJ Derraugh, J Carpinone & SM Bertram 2011. Post-plasmogamic pre-karyogamic sexual
selection: mate chioce inside an egg cell. Ideas in Ecology and Evolution 4:14-23. doi:
10.4033/iee.2011.4.3.n
The authors expand on the work of Carre and Sardet and develop a framework where postplasmogamic pre-karyogamic cryptic female choice is included.
Carré D & C Sardet 1984. Fertilisation and early development in Beroe ovate. Developmental biology
105:188-195.
In the ctenophore where polysperm are common, the female pronucleus moves between
sperm nucleus within the egg and chooses which sperm pronucleus to fuse with. Birkhead
and Pizzari (2002) provide amazing images of this very special cryptic female choice.
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Cryptic female choice in plants
Willson & Burley 1983, Delph & Havens 1998, and Moore & Pannell 2011 review and discuss how
gamete incompatibility and selection at the gamete-level can also occur in plants, which has been
demonstrated by Björkman 1995.
Willson MF & N Burley 1983. Mate choice in plants: tactics, mechanism and consequences.
Princeton, N.J.: Princeton University Press.
The book reviews sexual selection in plants discussing male-female interactions affecting
reproduction.
Björkman T 1995. The effectiveness of heterostyly in preventing illegitimate pollination in dish-shaped
flowers. Sexual Plant Reproduction 8:143–146.
The study shows bias in favour of compatible pollination in the plant Fagopyrum esculentum.
Delph LF & K Havens 1998. Pollen competition in flowering plants. In Birkhead TR & AP Møller (eds)
Sperm competition and sexual selection. Academic Press London.
The chapter written by Delph and Havens in Birkhead & Møller’s book (1998) discusses ‘postcopulatory’ sexual selection in plants.
Moore JC & JR Pannell 2011. Sexual selection in plants. Current Biology 21:R176-R182.
A review on sexual selection in plants, including selection after pollination.
Theoretical models including cryptic female choice
Compared to other episodes of sexual selection (e.g. sperm competition), there is very little
theoretical work done modelling aspects of cryptic female choice. Kuijper et al 2012 presents an
overview of models on sexual selection including post-copulatory mate choice. There are some
models on how males should respond in terms of ejaculate investment, if females perform postcopulatory biases, for example models by Parker 1998, Greeff & Parker 2000, Ball & Parker 2003,
and Holman & Snook 2006. Fromhage et al 2008 includes female influences on male post-copulatory
strategies, and Van Velzen et al 2009 discuss the influence of cryptic female choice on sex allocation
in hermaphrodites.
Parker GA 1998. Sperm competition and the evolution of ejaculates: Towards a theory base. In
Birkhead TR & AP Møller (eds) Sperm competition and sexual selection. Academic Press London.
Parker gives a great overview of theoretical models mainly on male responses to female
polyandry and sperm competition. Some mechanisms that could function as a cryptic female
choice are presented.
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Kuijper B, I Pen & FJ Weissing 2012. A guide to sexual selection theory. Annual Reviews in Ecology
Evolution and Systematics 43:287–311. doi: 10.1146/annurev-ecolsys-110411-160245.
A global overview of theoretical models on sexual selection, including post-copulatory mate
choice.
Fromhage L, J McNamara & A Houston 2008. Sperm allocation strategies and female resistance: a
unifying perspective. American Naturalist 172:25–33.
A game theory model investigating female resistance to excessive matings and the
consequences the female responses have for male sperm allocation strategies.
Van Velzen E, Scharer L & I Pen 2009. The effect of cryptic female choice on sex allocation in
simultaneous hermaphrodites. Proceedings of the Royal Society of London B 276:3123-3131. doi:
10.1098/rspb.2009.0566.
A model studying the coevolution of cryptic female choice and sex allocation in simultaneous
hermaphrodites, showing that the mechanism of cryptic female choice affects sex allocation.
Olsson M, M Pagel, R Shine, T Madsen, C Doums, A Gullberg & H Tegelström 1999. Sperm choice
and sperm competition: suggestions for field ad laboratory studies. Oikos 84:172-175.
The paper presents a model aiming to enable estimation of the potential confounding effect of
relatedness-related reduction in fitness, when investigating patterns of post-copulatory sexual
selection.
Greeff JM & GA Parker 2000. Spermicide by females: what should males do? Proceedings of the
Royal Society of London B 267:1759–1763.
The paper models how males should respond to female spermicide, and show that
spermicide can select for the production of additional sperm to compensate for the sperm that
die.
Ball MA & GA Parker 2003. Sperm competition games: sperm selection by females. Journal of
Theoretical Biology 224:27-42. doi: 10.1016/S0022-5193(03)00118-8.
The authors model evolutionary games on male sperm allocation in favoured and unflavoured
games when females operate sperm selection.
Holman L & RR Snook 2006. Spermicide, cryptic female choice and evolution of sperm form and
function. Journal of Evolutionary Biology 19:1660-1670. doi: 10.1111/j.1420-9101.2006.01112.x.
Holman and Snook’s models show that under some circumstances parasperm may evolve
because they dilute the effects of female mechanisms that kill eusperm (spermicide), thereby
providing an advantage in sperm competition.
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