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Genetic conflict, kin and the origins of
novel genetic systems
Benjamin B. Normark1 and Laura Ross2
rstb.royalsocietypublishing.org
Review
Cite this article: Normark BB, Ross L. 2014
Genetic conflict, kin and the origins of novel
genetic systems. Phil. Trans. R. Soc. B 369:
20130364.
http://dx.doi.org/10.1098/rstb.2013.0364
One contribution of 14 to a Theme Issue
‘Inclusive fitness: 50 years on’.
Subject Areas:
evolution, genetics, ecology,
theoretical biology
Keywords:
endosymbiont, Wolbachia, genetic system,
haplodiploidy, parthenogenesis
Author for correspondence:
Benjamin B. Normark
e-mail: [email protected]
1
Department of Biology and Graduate Program in Organismic and Evolutionary Biology, University of
Massachusetts, Amherst, MA 01003, USA
2
School of Biological Sciences, Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3JT, UK
Genetic conflict may have played an important role in the evolution of novel
genetic systems. The ancestral system of eumendelian genetics is highly
symmetrical. Those derived from it (e.g. thelytokous parthenogenesis, haplodiploidy and parent-specific allele expression) are more asymmetrical in the
genetic role played by maternal versus paternal alleles. These asymmetries
may have arisen from maternal–paternal genetic conflict, or cytonuclear conflict, or from an interaction between them. Asymmetric genetic systems are
much more common in terrestrial and freshwater taxa than in marine taxa.
We suggest three reasons for this, based on the relative inhospitability of terrestrial environments to three types of organism: (i) pathogens—departure
from the marine realm meant escape from many pathogens and parasites,
reducing the need for sexual reproduction; (ii) symbionts—symbionts are no
more important in the terrestrial realm than the marine realm but are more
likely to be obligately intracellular and vertically transmitted, making them
more likely to disrupt their host’s genetic systems; (iii) Gametes and
embryos—because neither gametes nor embryos can be shed into air as
easily as into seawater, the mother’s body is a more important environment
for both types of organisms in the terrestrial realm than in the marine realm.
This environment of asymmetric kinship (with neighbours more closely
related by maternal alleles than by paternal alleles) may have helped to
drive asymmetries in expression and transmission.
1. Introduction
Meiosis is a fair lottery: each allele in a diploid genome has the same probability
of being passed on to the next generation. Asymmetry in transmission probability between alleles at a locus—meiotic drive—evolves frequently in some
taxa but in most cases is quickly suppressed [1,2]. But one kind of genetic asymmetry can be persistent, and that is asymmetry between males and females,
which is seen in unusual genetic systems such as haplodiploidy and parthenogenesis (figure 1). The origin and distribution of these asymmetric genetic
systems remains poorly understood. In this review, we discuss conflicts
between maternal and paternal alleles, as well as between nuclear and cytoplasmic genes, and consider the extent to which each of these might have
been important in the evolution of asymmetric genetic systems. We also consider interactions among relatives, and how indirect fitness may have affected
the evolution of asymmetric reproductive systems. Finally, we consider the distribution of these systems across habitats and consider the question of why
asymmetric genetic systems occur mainly in terrestrial and freshwater rather
than marine habitats.
2. Ancestral symmetry, novel asymmetry
Most eukaryotes reproduce sexually, with two gamete types: egg and sperm.
Although there is a large size asymmetry between egg and sperm, in most
eukaryotes they play symmetrical genetic roles. In the ancestral ‘eumendelian’
genetic system of eukaryotes, an allele contributed by a sperm cell has the same
& 2014 The Author(s) Published by the Royal Society. All rights reserved.
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gametes
embryos
offspring
parthenogenesis
automixis
apomixis
gynogenesis
father’s genes
eliminated
from germline
sperm present
arrhenotoky
PGE
father’s
genes
eliminated
androgenesis
cyclic
parthenogenesis
asexual generation
sexual generation
Figure 1. Asymmetric genetic systems, where the sperm and egg genome have different roles or fates [3 – 11]. Each row of this figure describes a different
asymmetric genetic system. The first column of each row shows the adult generation, the second column the gametes produced, the third column the embryos
shortly after fertilization and the last column the offspring generation. The animal symbols represent males (in blue) and females (in red). Haploid individuals and
gametes are shown with one chromosome. Diploid individuals and gametes are shown with two chromosomes. From top to bottom: Parthenogenesis ¼ obligate
thelytokous parthenogenesis, development of females from unfertilized eggs (including apomixis ¼ egg production by mitosis and automixis ¼ egg production
involving meiosis). A few thousand eukaryote species, especially freshwater and terrestrial animals. Gynogenesis ¼ development of females from fertilized eggs,
but with only the mother’s genome. Many groups including salamanders, fish, insects and angiosperms. Hybridogenesis ¼ gynogenesis, except that the paternal
genome is incorporated and expressed in the offspring but later eliminated from the offspring’s germline. Several species of fish and frogs. Arrhenotoky ¼ arrhenotokous haplodiploidy or haplodiploidy in the strict sense, development of males from unfertilized eggs. Males are haploid and never have a paternal genome at
all. Several groups of insects and mites, oxyurid nematodes and monogonont rotifers. PGE ¼ paternal genome elimination, development of males from fertilized
eggs in which males have a paternal genome but do not transmit it. Males may lose their paternal genome either early in development, becoming haploid (early
PGE) or retain their paternal genome without transmitting it (late PGE). A few groups of insects, mites and springtails. Androgenesis ¼ development of either sex
from fertilized eggs in which the sperm genome supplants egg genome. Offspring have the father’s nuclear genome. A few clam species and Saharan cypress. Cyclic
parthenogenesis ¼ system in which one or more parthenogenetic generations regularly alternates with a sexual generation. Several groups including cladocera,
monogonont rotifers, some loriciferans and several groups of insects.
fate as one contributed by an ovum: an identical chance of
transmission to offspring, as mediated by the meiotic lottery.
But this ancestral system is not universal. Less-symmetrical
genetic systems have arisen many times in the history of
life (figure 1 and table 1). Novel genetic systems disrupt
early embryonic development and are likely to impose initial
viability costs on embryos [15]. This has been shown empirically in insects, where many species are able to lay occasional
Phil. Trans. R. Soc. B 369: 20130364
from other sp.
hybridogenesis
from other sp.
2
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sperm absent
parents
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Table 1. Asymmetric genetic systems across animal phyla. Information from Jarne & Auld [12], Hughes [13] and Bell [5]. Non-marine taxa from each order are
in italics, while marine taxa are described in roman font.
marine/non-marine
parthenogenesis
other asymmetric reproduction
Annelida
marine
2
none
Annelida
non-marine
þ
sperm-dependent parthenogenesis
Arthropoda
marine
2
none
Arthropoda
non-marine
þ
parent-specific allele expression, gynogenesis, hybridogenesis,
arrhenotoky, PGE, cyclic parthenogenesis
2
none
Cephalochordata
marine
2
none
Chaetognatha
marine
2
none
Cnidaria
marine
rare
none
Ctenophora
marine
2
none
Cycliophora
marine
2
none
Echinodermata
marine
rare
none
a
Ectoprocta (Bryozoa)
marine
2
none
Ectoprocta (Bryozoa)
non-marine
2
none
Entoprocta
marine
2
none
Gastrotricha
marine
rare
none
Gastrotricha
non-marine
þ
none
Gnathostomulida
marine
2
none
Hemichordata
marine
2
none
Kinorhyncha
marine
2
none
Loricifera
marine
2
cyclic parthenogenesis
Mesozoa
marine
2
none
Mollusca
marine
rare
sperm-dependent parthenogenesisa
Mollusca
non-marine
þ
androgenesis a
Nematoda
marine
rare
none
Nematoda
non-marine
þ
sperm-dependent parthenogenesis, cyclic parthenogenesis, arrhenotoky
Nematomorpha
non-marine
þ
none
Nemertea
marine
2
none
Nemertea
non-marine
2
none
Onychophora
non-marine
rare
none
Pentastomida
non-marine
2
none
Phoronida
marine
2
none
Phoronida
marine
2
none
Platyhelminths
marine
2
none
Platyhelminths
non-marine
þ
sperm-dependent parthenogenesis
Porifera
marine
2
none
Priapulida
marine
2
none
Rotifera
non-marine
þ
cyclic parthenogenesis, arrhenotoky
Rotifera
marine
2
none
Sipuncula
marine
rare
none
Tardigrada
marine
2
none
Tardigrada
non-marine
þ
none
Urochordata
marine
2
none
Vertebrata
marine
2
none
Vertebrata
non-marine
þ
parent-specific allele expression, gynogenesis, hybridogenesis
An unusual inheritance pattern of mitochondria has evolved multiple times both in marine and freshwater molluscs. Here, females transmit their mitochondria to
both their male and female offspring, whereas males transmit their mitochondria only through sons [14].
Phil. Trans. R. Soc. B 369: 20130364
marine
Brachiopoda
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phylum
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3. Genetic conflict in the nucleus: maternal
versus paternal alleles
4. Cytonuclear conflict and inclusive fitness of
intracellular bacteria
Although the genetics of the nucleus is usually highly symmetrical, there is typically an enormous asymmetry between the two
sexes in cytoplasmic inheritance. The egg has a much greater
volume of cytoplasm than the sperm and usually includes cytoplasmic elements that have their own genome. As a result, these
cytoplasmic genomes are only transmitted through females.
Some authors draw a hard distinction between cytonuclear
genetic conflict involving organelles, on the one hand, and
host–symbiont conflict involving intracellular bacteria, on the
other [3]. But in our view, this dichotomy obscures more than
it illuminates. Many insects are utterly dependent upon their
primary bacterial endosymbionts, some of which have been vertically transmitted within their hosts for hundreds of millions
of years, losing a large majority of their genes and becoming
effectively organelle-like [31]. Compared with them, the plant
mitochondrial genome often has a much larger genome size
and much higher rates of gene rearrangement, and indeed, the
plant mitochondrial genome often causes cytoplasmic male
sterility, analogous to the male-killing engaged in by intracellular bacteria [32]. Instead of a dichotomy, we see a diverse
continuum, with animal mitochondria and ancient reducedgenome symbionts at one (well-behaved mutualist) end of the
spectrum, and frequently swapped reproduction manipulators
like Cardinium and Wolbachia at the other (parasitic) end, with
plant mitochondria and an enormous variety of other bacteria
in between [31,33–38]. The aggregate of all the maternally transmitted genomes in a cell can be viewed as a single ‘cytogenome’
with near-complete genetic linkage and a unified interest in
skewing the sex ratio towards females. Here, we treat the sex
ratio conflict between the nucleus and the entire cytogenome
as a form of genetic conflict.
Bacteria that invade the cytoplasm of multicellular organisms acquire a population structure that mirrors that of the
cells they have invaded: differentiation of the host’s cells into
germline and soma often imposes something very much like
a germline/soma distinction upon the resident bacterial
lineage. It is a remarkable natural experiment that has been
repeated many times: when you impose multicellularity and
germline sequestration on a unicellular organism, do its sterile
members—its potential ‘soma’—evolve somatic functions that
enhance the fitness of its germline? In most respects, the predicted optimal phenotype of both bacterial and host genomes
is the same—maximal fitness of infected hosts—leading to
tight integration of host and bacterial physiology and few
insights into bacterium-specific selection. But there is one
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Selfish genetic elements favour their own direct or indirect
fitness while sacrificing the fitness of other genetic elements
residing in the same genome. A selfish genetic element might
mediate a transition to a novel genetic system that favours
the element, even at a cost to organismal fitness. Consider the
haplodiploid systems, in the broad sense: those in which
males transmit only the alleles they received from their mothers
(figure 1). Most scale insects have a system of late paternal genome elimination [18] in which males are diploid but
the chromosomes that a male received from his father are
heterochromatic. When sperm are formed, the maternal
chromosomes are packaged into the sperm while the paternal
chromosomes are left behind [19,20]. S. W. Brown, observing
this system 50 years ago, noted its similarity to meiotic drive
[21], and showed that a gene expressed in females that causes
paternal chromosome elimination would spread rapidly
through a population. Arrhenotoky—parthenogenetic production of haploid male offspring (figure 1)—evokes conflict
less vividly than does the physical destruction of paternal
chromosomes, but it has identical transmission genetics and
confers an identical advantage if caused by a gene expressed
in females [15,22]. Even if haploid males have relatively low
viability compared with diploid males, an allele causing haplodiploidy can still invade (as long as haploid male viability is
more than 50% diploid male viability). Ever since Brown,
most models of haplodiploidy have followed his in invoking
a transmission advantage for maternal alleles at the expense
of paternal alleles, essentially viewing haplodiploidy as an outcome of maternal-allele victory in a conflict with paternal
alleles over transmission by males [3,15,23–28].
Usually, asymmetric genetic systems are those in which the
role of the male is reduced. Either males are excluded from
parentage of sons (haplodiploidy), or they are excluded from
some generations (cyclic parthenogenesis) or they are simply
eliminated altogether (thelytokous parthenogenesis; figure 1).
Perhaps Brown’s insight can be generalized and we can view
the origins of such systems as instances of maternal victory
in a maternal–paternal conflict over transmission. It is not
entirely clear why females are typically the victors in these conflicts, but it is plausible that, in crude terms, when the sperm
and egg fight the egg usually wins because it is bigger [29].
Females deposit many more gene products that males into
the zygote and do so earlier, and therefore may be at an advantage in affecting the outcome of the interaction. Indeed most
such systems feature parthenogenesis, in which sperm are
excluded from the ovum altogether.
In a few cases, the asymmetry runs the other way, with
an expanded role for males and a reduced role for females.
The most dramatic case of this is androgenesis (figure 1), in
which the nuclear genome of the sperm cell entirely supplants
that of the egg, resulting in clonal reproduction via sperm
[4]. Another system in which males may strongly influence
outcomes is parent-specific allele expression—or ‘genomic
imprinting’ as it is often simply called, though genomic imprinting also underlies paternal genome elimination. Parent-specific
allele expression in mammals and angiosperms affects only
the expression of genes and does not directly affect their
transmission, although by affecting maternal and offspring
survivorship and reproduction it indirectly influences transmission. In placental mammals, the paternal allele in an embryo
often has a pattern of expression that results in a relatively
high rate of nutrient transfer from mother to embryo, while
the maternal allele often has a pattern of expression that results
in a lower rate of nutrient transfer [30]—paternal alleles are
‘greedier’ for maternal resources, as they are less related to the
mother and to her other offspring.
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parthenogenetic eggs, but where there is often a significantly
reduced fitness for embryos developing from unfertilized eggs
compared with those developing from fertilized eggs [16,17].
So, if transitions to new genetic systems reduce organismal
fitness, at least initially, then why do they occur?
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5
reproductive manipulations that enhance direct fitness of bacteria
(b)
direct
transmission
male from
unfertilized egg
female from
unfertilized egg
horizontal
transmission
direct
transmission
direct
transmission
female from
fertilized egg
reproductive manipulations that enhance indirect fitness of bacteria
(c)
(d)
dead male
embryo
indirect fitness
benefit
indirect fitness
benefit to
infected females
sisters
dead uninfected offspring
Figure 2. Adaptations of intracellular bacteria to increase their direct or indirect fitness by manipulating the reproduction of their host. Direct effects of endosymbiont
(including reproductive manipulation and transmission) are indicated with solid arrows, while indirect effects that benefit related endosymbionts in different hosts are
indicated with dashed arrows. Diploid individuals are represented by male or female symbols with two chromosomes. Haploid males are represented by a male symbol
with one chromosome. The infection status of an individual is indicated by the presence of the red Wolbachia icon. (a) Feminization, conversion of males into females,
here including feminization of parthenogenetically produced males (often referred to as ‘parthenogenesis-induction’; example Encarsia pergandiella, photo by Alex Wild),
as well as feminization of sexually produced males (example Armadillidium vulgare, photo by Franco Folini). (b) Late male-killing, killing of males late in development,
such that dead males can serve as a source of infection of nearby females (example Culex tarsalis, photo by Joseph Berger, Bugwood.org). (c) Early male-killing (EMK),
killing of male embryos. When there is competition between host siblings, EMK enhances fitness of the bacterial clone inhabiting a single host individual (example
Harmonia axyridis, photo by Alex Wild). (d) CI, modification of sperm to kill uninfected eggs. Infected eggs are rescued by an antitoxin. CI enhances the fitness of the
bacterial clone(s) encoding compatible antitoxins (example Nasonia vitripennis, photo by Gernot Kunz).
major source of conflict between the nucleus and the cytogenome: males. Male offspring represent half of the nucleus’s
direct fitness, but cytoplasmic elements in males have no
direct fitness. This creates a permanent conflict of interest
over male fitness—the nucleus is under selection to maximize
the fitness of both males and females, whereas the cytogenome
is under selection to maximize the fitness of females only.
Accordingly, elements within the cytogenome have evolved
various means of sacrificing male fitness in favour of female fitness. According to almost all accounts, there are four such
means: feminization, parthenogenesis-induction, male killing
and cytoplasmic incompatibility (CI) [33,39–41]. This standard
four-part taxonomy obscures a more fundamental dichotomy
between selfish versus cooperative phenotypes of cytoplasmic
elements (figure 2). For a maternally transmitted bacterium in
a male host, there are two different ways it can enhance its fitness: it can gain direct fitness by regaining access to a female
germline or it can gain indirect fitness by enhancing the reproductive success of its clone-mates housed in the female
germline. Bacterial lineages that take the first route—regain of
direct fitness—benefit themselves as individual cells. They
remain unicellular organisms in terms of the level at which
selection acts on them. But bacteria that take the second
route—gain of indirect fitness—become essentially multicellular
organisms with a germline and an adaptively functional soma.
For obligately intracellular bacteria that need to be transmitted vertically, there appears to be only one means of regaining
direct fitness in the host’s male germline: feminization of the
host. There is a large literature devoted to ‘parthenogenesisinduction’ by intracellular bacteria as a phenomenon different
from feminization, but this is a misnomer. ‘Parthenogenesisinduction’ has been reliably demonstrated only in groups that
have parthenogenetically produced males, and it consists of the
conversion of parthenogenetically produced males into females
[42–45]. Thus, it is simply feminization. Of course, feminization
has very different long-term consequences when it occurs in a
population in which males are produced parthenogenetically
compared to one in which all individuals are produced sexually:
in populations with parthenogenetically produced males, feminizers can confer short-term fitness benefits and can be found at
100% frequency; in populations with sexually produced males,
feminizers impose bigger fitness costs and cannot reach 100% frequency without causing local population extinction. There is also
usually a mechanistic difference. Feminizing bacteria in sexually
Phil. Trans. R. Soc. B 369: 20130364
male from
fertilized egg
dead male larvae
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(a)
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We have discussed conflict between the nucleus and the cytogenome, and how elements within the cytogenome have
(a) Parthenogenesis
The clearest case of genetic conflict leading to the evolution of a
novel genetic system is that of feminizing bacteria converting
arrhenotoky (figure 1) to thelytokous parthenogenesis (parthenogenetic production of females), which has been documented
in several species of wasps and thrips [42–45,55]. Origins of
obligate thelytokous parthenogenesis are probably the most
frequently occurring evolutionary transition between genetic
systems in nature. Are cytoplasmic elements often the instigators of these transitions? At this point, there is little evidence
that they are. Well-documented cases are limited to parasitic
wasps and thrips, and there are many parthenogenetic lineages
in which no intracellular bacteria have been detected [56,57].
There are some cases in groups other than parasitic wasps
in which parthenogenetic lineages are Wolbachia or Cardinium
infected while related sexual lineages are not [58,59]. These
are sometimes seen as apparent cases of parthenogenesisinduction, but it is also possible that parthenogenesis in these
cases is a host-mediated response to a shortage of males
resulting from bacterium-induced male-killing or feminization.
More broadly, there are several ways in which genetic conflict could lead to origins of parthenogenesis. Genetic conflict
elevates the cost of sex [60], which may contribute to enabling
parthenogenetic lineages to outcompete sexual ones [29]. In
aquatic invertebrates, parthenogenesis arises more frequently
in groups that brood their young [61]. It has been suggested
that the viability costs of the origin of a new genetic system
are reduced in brooders, because resources that would have
been used by aborted embryos can be used by their siblings
instead [61]. This same phenomenon—resource competition
among siblings—can increase the intensity of genetic conflict,
as seen in the emergence of male-killing in intracellular bacteria
inhabiting hosts with sibling competition, and hence increase
the cost of sex. On the whole, the evidence that genetic conflict
is an important cause of the origins of parthenogenetic lineages
is weak. The many other costs of sex ensure that there is a broad
parameter space in which newly arising parthenogenetic
lineages can thrive, at least in the short term [5,60]. Genetic conflict may have been more important in the origins of the other,
more obviously asymmetric genetic systems, in which there is
an ongoing, unequal role for males.
(b) Haplodiploidy
The hypothesis that conflict between maternal and paternal
alleles has led to haplodiploidy runs into the difficulty of
explaining why haplodiploidy has arisen in only certain
groups and not others. Hamilton noted that haplodiploidy
arises in groups that have gregarious broods [62,63] and maternally transmitted endosymbionts [64]. Normark [28] pointed
out that this combination of features leads to male-killing endosymbionts and speculated that male haploidy may have arisen
as a male-killing endosymbiont phenotype that was later
coopted by the maternal genome in the host. Engelstädter &
Hurst [65] pointed out that CI bacteria often effectively haploidize embryos and that these might have played a role in the
origins of viable haploid males. Jack Werren has suggested
an alternative route for the origin of arrhenotokous haplodiploidy from an ancestral population beset by male-killers.
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5. Intracellular bacteria and the origins of
asymmetric genetic systems
evolved a number of ways to manipulate reproduction. But
the question remains: does this reproductive manipulation
lead to the origin of novel genetic systems?
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produced male zygotes induce development of a female
phenotype, without changing the genotype [46,47]. In parthenogenetically produced males, on the other hand, the most
commonly employed means of feminization is diploidization of
the haploid zygote, resulting in an individual that is both genetically and phenotypically female [48]. But exceptions are known,
highlighting the falseness of the distinction between feminization
and ‘parthenogenesis-induction’: in the mite genus Brevipalpus,
Cardinium bacteria cause parthenogenetically produced males
to develop as females, though they remain haploid and thus
genetically male [49,50].
For bacteria that can be either vertically or horizontally
transmitted, bacteria in males may be able to reproduce if
they can be transmitted horizontally. Such bacteria rarely
affect host sex ratio, but a few are known to induce late
male-killing: proliferation of bacteria in males after they
reach a large body size, with the dead male then serving as
a source of horizontal transmission [51] (figure 2).
Bacteria that can induce feminization or late male-killing
gain a direct-fitness benefit. But other adaptations of intracellular bacteria to the male germline have evolved in spite of the fact
that they do not enhance the direct fitness of the bacteria, only
their indirect fitness. One such adaptation is early male-killing
(EMK), which might also be called immediate suicide. At a very
early stage in embryogenesis—plausibly, as soon as the bacteria
detect a cue indicating that they are in a male rather than a
female—bacteria in male embryos kill themselves and their
host. Male-killing evolves in bacteria inhabiting hosts with
gregarious broods, often with inter-sibling cannibalism, such
that the death of one sibling benefits surviving siblings [51].
Under these circumstances, suicidal male-killing bacteria
benefit their clone-mates residing in the males’ sisters and
thus enhances the indirect fitness of the male-killers [51,52].
In some lineages of intracellular bacteria, cells inhabiting
the host’s male germline have taken on a much more elaborate
somatic function: cytoplasmic incompatibility (CI) [53]. The
precise mechanisms of CI are not well known, but its effects
can be intuitively understood by imagining that bacteria in
the male germline secrete a poison that is incorporated into
sperm, while their clone-mates in the female germline secrete
an antidote that is incorporated into eggs [54]. Sperm deliver
the poison when fertilizing an egg, and zygotes containing
the poison but not the antidote do not survive. Thus, infected
males destroy uninfected eggs, while successfully fertilizing
infected eggs. An infected male also destroys eggs infected
with other strains of bacteria, if they are incompatible with
the strain that he carries. Whereas male-killing benefits very
close clone-mates (derived from the same host female a
single host generation ago), CI benefits a much broader pool
of clone-mates across the population. Indeed in the case of
the killing of uninfected eggs, the CI phenotype benefits the
entire guild of intracellular bacteria. Inter-clone battles
emerge when CI sperm destroy eggs infected by incompatible
bacterial clones, but within-clone compatibility persists for
many generations in laboratory culture, indicating that the service provided by bacteria in CI males benefits quite distant kin.
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Although better comparative evidence is still needed, it
appears that species with brood chambers in which maternal
kin interact are more likely to give rise to novel asymmetric
genetic systems. This is apparently true of parthenogenesis
[61], haplodiploidy [28] and parent-specific allele expression
[67]. There are at least two possible reasons why this might
be so. One is that the death of one embryo in a brood chamber
can benefit its siblings. This reduces the cost of viabilitylowering innovations, for example novel genetic systems [61].
It also makes minimum male viability the adaptive optimum
for the cytogenome, creating a cytonuclear conflict over male
viability that can drive the evolution of novelties relating to
sex allocation and sex determination [28]. The second reason
why brood chambers may lead to novel genetic systems is
asymmetric relatedness. If the mother is the parent that establishes the brood chamber, all the offspring in the brood are
maternally related, though they may not all be paternally
related. An additional layer of asymmetric relatedness holds
if the brood chamber is the mother’s body, as all of the offspring are related to her through their maternal genes,
though none (under outcrossing) are related to her by their
paternal genes. This relatedness asymmetry has apparently
led to the evolution of parent-specific allele expression in mammals [67]. In mammals, paternally expressed alleles in the
embryo typically have a greedy phenotype, benefitting the
embryo but imposing fitness costs on maternal kin. Parentspecific allele expression with greedy paternally imprinted
phenotypes may have arisen in other taxa as well, and asymmetric genetic systems that limit the role of the paternal
genome may evolved in response to this [29].
Thus, we can identify three effects of indirect fitness that
may have played a role in the origins of novel genetic systems.
First, novel genetic systems have often arisen in situations in
which the direct-fitness costs of early embryo mortality are
compensated in part by indirect-fitness benefits. Second,
novel genetic systems have often arisen under conditions of
asymmetric relatedness, such that indirect-fitness costs and
benefits are disproportionately due to effects on maternal
rather than paternal kin. This may have led to a divergence
in optimal phenotype between maternally versus paternally
inherited alleles, which may have led in turn to differentiation
in the roles played by maternal and paternal alleles in the genetic system. Finally, novel genetic systems have often arisen in
animals whose cytoplasm contains maternally inherited bacteria that are deprived of direct fitness in male hosts. Some of
7. Ecology of asymmetric kin and asymmetric
genetics: the big picture
Asymmetric genetic systems occur in terrestrial and freshwater
environments. They appear to be exceedingly rare in marine
environments (table 1). This pattern has probably been exaggerated by observational bias, as terrestrial and freshwater
organisms are often more amenable to study than marine
organisms. But enough is known about marine organisms
that the pattern is unlikely to be entirely artefactual [68,69].
The pattern is a striking feature of the distribution of genetic
systems on earth, albeit one that has rarely been remarked
upon. The marine environment is presumably the one in
which sex and symmetrical genetics evolved, and they are
apparently all but indispensable in that environment. The
repeated invasion of the novel environments of land and freshwater repeatedly gave rise to novel, less-symmetrical genetic
systems. Why should this be so? Marine organisms dwell
within the medium in which life evolved and to which all life,
until relatively recently, was adapted. We propose that the distribution of genetic systems has been shaped by seawater’s
suitability for four classes of organisms in particular: pathogens, symbionts, gametes and embryos. Air, subjected to
constant UV radiation, is a persistently challenging medium
for the survival and dispersal of any of them. Freshwater,
too, is constantly being distilled by the hydrologic cycle and
subjected to greater thermal fluctuations and other abiotic variations than marine habitats, making it, too, a more challenging
medium than seawater.
(a) Pathogens: the Red Queen rules the waves
Viruses are an abundant component of seawater [70]. This
may help to explain one aspect of the distribution of genetic
systems: the near-absence of obligate parthenogenesis from
marine environments, in comparison to reasonably high frequency in some terrestrial and freshwater environments
(table 1). This observation may be understandable in terms
of the Parasite Red Queen hypothesis for the adaptive significance of sex [71,72]. When we left the ocean, we may have left
most of our pathogens and parasites behind and thus are less
reliant on sex than marine organisms are.
(b) Symbionts: the Trojan microbiota
Symbiosis between animals and microorganisms is probably at
least as important in marine environments as in terrestrial and
freshwater environments, as illustrated dramatically by corals
[73,74]. But in marine environments, microbial symbionts are
more often transmitted horizontally and acquired from the
environment by each generation of animals [75]. In terrestrial
environments in particular, vertical transmission of microbial
endosymbionts is much more common, possibly because
air is such a poor medium for symbiont transmission, such
that a large percentage of terrestrial species carry maternally
transmitted endosymbionts [31,36,76]. Such symbionts may
engage in conflicts with their host’s genome over sex determination and male viability, de-stabilizing their hosts’ genetic
7
Phil. Trans. R. Soc. B 369: 20130364
6. Interactions among relatives, indirect fitness
and origins of novel genetic systems
these bacteria may have evolved to enhance their indirect fitness via ‘somatic’ phenotypes, for example male-killing, and
these may have played a role in altering the role of males in
the host’s genetic system.
rstb.royalsocietypublishing.org
When male-killers are at high frequency, there is strong selection to produce offspring parthenogenetically (as many
females go unmated) and to produce male offspring (as these
are rare and have extraordinary mating opportunities). Thus,
the parthenogenetic production of male offspring would be
strongly favoured by selection in a population in which
male-killers are at high frequency, and this might have led to
the direct origin of arrhenotoky in the uninfected segment of
the population (J. H. Werren 2004, personal communication).
To date, there is no direct empirical support for a role of endosymbionts in the evolution of haplodiploidy, although the
presence of endosymbionts is correlated with haplodiploidy
in scale insects [66].
Downloaded from http://rstb.royalsocietypublishing.org/ on May 10, 2017
of cytoplasmic male sterility) and have frequently originated
asymmetric genetic systems including apomixis, gynogenesis
(pseudogamy) and parent-specific allele expression.
8. Conclusion
(c) Gametes and embryos: both blood and water are
thicker than air
Acknowledgements. For inspiration and encouragement, we thank Jon
Seger, Robert Trivers, Jack Werren, David Haig and Andy Gardner.
For comments on a previous draft that improved the manuscript,
we thank Stuart West and two anonymous reviewers.
Funding statement. Our collaboration benefited from travel funding provided by the Royal Entomological Society, the National Evolutionary
Synthesis Center (NESCent) and NSF (DEB-1258001 to B.B.N.). L.R. is
financially supported by NERC.
References
1.
2.
3.
4.
5.
6.
7.
Leigh Jr EG. 1971 Adaptation and diversity.
San Francisco, CA: Freeman, Cooper.
McDermott SR, Noor MA. 2010 The role of
meiotic drive in hybrid male sterility. Phil.
Trans. R. Soc. B 365, 1265– 1272. (doi:10.1098/rstb.
2009.0264)
Burt A, Trivers R. 2006 Genes in conflict: the biology
of selfish genetic elements. Cambridge, MA: Harvard
University Press.
McKone MJ, Halpern SL. 2003 The evolution of
androgenesis. Am. Nat. 161, 641–656. (doi:10.
1086/368291)
Bell G. 1982 The masterpiece of nature. Berkeley, CA:
University of California Press.
Bull JJ. 1983 Evolution of sex determining
mechanisms. Menlo Park, CA: Benjamin/Cummings.
Hebert PDN. 1987 Genotypic characteristics of cyclic
parthenogens and their obligately asexual
derivatives. In The evolution of sex and its
consequences (ed. SJ Stearns), pp. 175–195. Basel,
Switzerland: Birhäuser Verlag.
8. Beukeboom LW, Vrijenhoek RC. 1998 Evolutionary
genetics and ecology of sperm-dependent
parthenogenesis. J. Evol. Biol. 11, 755–782.
(doi:10.1046/j.1420-9101.1998.11060755.x)
9. Normark BB. 2003 The evolution of alternative
genetic systems in insects. Annu. Rev. Entomol. 48,
397 –423. (doi:10.1146/annurev.ento.48.091801.
112703)
10. Fournier D, Estoup A, Orivel J, Foucaud J, Jourdan H,
Breton JL, Keller L. 2005 Clonal reproduction by
males and females in the little fire ant. Nature 435,
1230 –1234. (doi:10.1038/nature03705)
11. Schlupp I. 2005 The evolutionary ecology of
gynogenesis. Annu. Rev. Ecol. Syst. 36, 399–417.
(doi:10.1146/annurev.ecolsys.36.102003.152629)
12. Jarne P, Auld JR. 2006 Animals mix it up too: the
distribution of self-fertilization among
13.
14.
15.
16.
17.
hermaphroditic animals. Evolution 60, 1816–1824.
(doi:10.1111/j.0014-3820.2006.tb00525.x)
Hughes RN. 1989 A functional biology of clonal
animals. Functional biology series. London, UK:
Chapman and Hall.
Hoeh WR, Stewart DT, Sutherland BW, Zouros E. 1996
Multiple origins of gender-associated mitochondrial
DNA lineages in bivalves (Mollusca: Bivalvia).
Evolution 50, 2276–2286. (doi:10.2307/2410697)
Bull JJ. 1979 An advantage for the evolution of male
haploidy and systems with similar genetic transmission.
Heredity 43, 361–381. (doi:10.1038/hdy.1979.88)
Corley LS, Moore AJ. 1999 Fitness of alternative modes
of reproduction: developmental constraints and the
evolutionary maintenance of sex. Proc. R. Soc. Lond. B
266, 471–476. (doi:10.1098/rspb.1999.0661)
Engelstadter J. 2008 Constraints on the evolution of
asexual reproduction. Bioessays 30, 1138– 1150.
(doi:10.1002/bies.20833)
Phil. Trans. R. Soc. B 369: 20130364
Shedding gametes into the water column is a successful
reproductive strategy for many completely sessile marine
organisms. No comparable strategy is available to terrestrial
organisms, as air is a poor medium for the propagation of
gametes. Embryos, likewise, can be shed into seawater but
cannot as easily be shed into air. Consequently, multicellular
terrestrial organisms are largely dependent upon internal
fertilization, and embryos often complete much of their development within a medium supplied by the mother, sometimes
within the mother’s own body. The mother, and maternal
kin, thus form a much more important part of the environment for terrestrial organisms than for marine organisms. This
asymmetric relatedness to neighbours produces asymmetric
selection on different components of the genome in terrestrial
organisms—for instance, favouring male-killing cytoplasmic
elements and greedy paternal alleles—which may play a role
in the origin of asymmetric genetic systems. It might appear
that terrestrial plants follow a marine-like strategy of shedding
gametes and embryos into the air, but this is not really the
case. Plants do not shed female gametophytes, only male gametophytes, so fertilization is still effectively internal within the
seed parent. Many plants shed fruits containing multiple maternally related embryos [77], and even a lone plant seed is far from
being a naked embryo: it usually consists primarily of endosperm, which often carries a double dose of the maternal
genome and single dose of the paternal genome, along with a
maternally derived integument. Thus plants, like terrestrial animals, have a maternal/paternal asymmetry in relatedness to
neighbouring tissues during early development, and, like terrestrial animals, have strong cytonuclear conflicts (e.g. origins
Symmetrical, eumendelian genetics is the genetics of fully
independent individuals. It is a system agnostic about kin,
in which information about the parental origin of each
allele is destroyed in each generation, with both parents’
alleles treated identically. This was the ancestral eukaryotic
sexual system that presumably arose in an isogamous unicellular lineage and that still characterizes the great majority of
eukaryotes. Novel, asymmetric genetic systems derived from
this ancestral system have arisen many times, especially in
multicellular organisms inhabiting terrestrial and freshwater
environments. The reasons for this are not clear, but one
important reason may be the greater role played by maternal
kin in environments relatively hostile to gametes and
embryos. Extended contact between mother and offspring
may facilitate all kinds of evolutionary novelties, by reducing
the cost of early abortion of a proportion of embryos [61]. In
particular, extended contact between maternal kin means that
the inclusive-fitness effects of maternal alleles will differ from
those of paternal alleles, and this may have led to the evolution of different roles and fates for maternal versus
paternal alleles [29,78]. The importance of maternal kin is
amplified further in environments hostile to unicellular symbionts, with the evolution of maternal channels of inheritance
for symbionts, which can then become highly disruptive of
their hosts’ sex determination systems.
8
rstb.royalsocietypublishing.org
systems. A few groups of marine invertebrates buck this trend
and have vertically transmitted symbionts: gutless oligochaetes, and solemyid and vesicomyid clams [75]. These are
promising systems to test the effects of endosymbionts on
host reproduction in a marine environment.
Downloaded from http://rstb.royalsocietypublishing.org/ on May 10, 2017
34.
35.
36.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47.
48.
49.
50.
51.
52.
53.
54.
55.
56.
57.
58.
59.
60.
61.
62.
isopods. In Insect symbiosis, vol. 3 (eds K Bourtzis,
TA Miller), pp. 273–294. Boca Raton, FL: CRC Press.
Cordaux R, Bouchon D, Greve P. 2011 The impact of
endosymbionts on the evolution of host sexdetermination mechanisms. Trends Genet. 27,
332–341. (doi:10.1016/j.tig.2011.05.002)
Weeks AR, Marec F, Breeuwer JAJ. 2001 A mite
species that consists entirely of haploid females.
Science 292, 2479– 2482. (doi:10.1126/science.
1060411)
Groot TVM, Breeuwer JAJ. 2006 Cardinium
symbionts induce haploid thelytoky in most clones
of three closely related Brevipalpus species. Exp.
Appl. Acarol. 39, 257 –271. (doi:10.1007/s10493006-9019-0)
Hurst LD. 1991 The incidences and evolution of
cytoplasmic male-killers. Proc. R. Soc. Lond. B 244,
91– 99. (doi:10.1098/rspb.1991.0056)
Hurst GD, Jiggins FM. 2000 Male-killing bacteria in
insects: mechanisms, incidence, and implications.
Emerg. Infect. Dis. 6, 329–336. (doi:10.3201/
eid0604.000402)
Engelstadter J, Telschow A. 2009 Cytoplasmic
incompatibility and host population structure.
Heredity 103, 196– 207. (doi:10.1038/hdy.2009.53)
Nor I, Engelstädter J, Duron O, Reuter M, Sagot M-F,
Charlat S. 2013 On the genetic architecture of
cytoplasmic incompatibility: inference from
phenotypic data. Am. Nat. 182, E15– E24.
(doi:10.1086/670612)
Arakaki N, Miyoshi T, Noda H. 2001 Wolbachiamediated parthenogenesis in the predatory thrips
Franklinothrips vespiformis (Thysanoptera: Insecta).
Proc. R. Soc. Lond. B 268, 1011– 1016. (doi:10.
1098/rspb.2001.1628)
Rabeling C, Kronauer DJ. 2013 Thelytokous
parthenogenesis in eusocial Hymenoptera. Annu.
Rev. Entomol. 58, 273–292. (doi:10.1146/annurevento-120811-153710)
Choleva L, Janko K. 2013 Rise and persistence of
animal polyploidy: evolutionary constraints and
potential. Cytogenet. Genome Res. 140, 151– 170.
(doi:10.1159/000353464)
Koivisto RKK, Braig HR. 2003 Microorganisms and
parthenogenesis. Biol. J. Linn. Soc. 79, 43 –58.
(doi:10.1046/j.1095-8312.2003.00185.x)
Provencher LM, Morse GE, Weeks AR, Normark BB.
2005 Parthenogenesis in the Aspidiotus nerii
complex (Hemiptera: Diaspididae): a single origin of
a worldwide, polyphagous lineage associated with
Cardinium bacteria. Ann. Entomol. Soc. Am. 98,
629–635. (doi:10.1603/00138746(2005)098[0629:PITANC]2.0.CO;2)
Lehtonen J, Jennions MD, Kokko H. 2012 The many
costs of sex. Trends Ecol. Evol. 27, 172– 178.
(doi:10.1016/j.tree.2011.09.016)
Lively CM, Johnson SG. 1994 Brooding and the
evolution of parthenogenesis: strategy models and
evidence from aquatic invertebrates. Proc. R. Soc.
Lond. B 256, 89– 95. (doi:10.1098/rspb.1994.0054)
Hamilton WD. 1967 Extraordinary sex ratios. Science
156, 477–488. (doi:10.1126/science.156.3774.477)
9
Phil. Trans. R. Soc. B 369: 20130364
37.
Rev. Microbiol. 6, 741 –751. (doi:10.1038/
nrmicro1969)
Perotti MA, Allen JM, Reed DL, Braig HR. 2007 Hostsymbiont interactions of the primary endosymbiont
of human head and body lice. FASEB J. 21,
1058 –1066. (doi:10.1096/fj.06-6808com)
Perlman SJ, Hunter MS, Zchori-Fein E. 2006 The
emerging diversity of Rickettsia. Proc. R. Soc. B 273,
2097 –2106. (doi:10.1098/rspb.2006.3541)
Zchori-Fein E, Perlman SJ. 2004 Distribution of the
bacterial symbiont Cardinium in arthropods. Mol.
Ecol. 13, 2009 –2016. (doi:10.1111/j.1365-294X.
2004.02203.x)
Anbutsu H, Fukatsu T. 2011 Spiroplasma as a model
insect endosymbiont. Environ. Microbiol. Rep. 3,
144 –153. (doi:10.1111/j.1758-2229.2010.00240.x)
Thao MLL, Baumann P. 2004 Evidence for multiple
acquisition of Arsephonus by whitefly species
(Sternorrhyncha: Aleyrodidae). Curr. Microbiol. 48,
140 –144. (doi:10.1007/s00284-003-4157-7)
Bandi C, Dunn AM, Hurst GD, Rigaud T. 2001
Inherited microorganisms, sex-specific virulence and
reproductive parasitism. Trends Parasitol. 17,
88 –94. (doi:10.1016/S1471-4922(00)01812-2)
Veneti Z et al. 2012 Loss of reproductive parasitism
following transfer of male-killing Wolbachia to
Drosophila melanogaster and Drosophila simulans.
Heredity 109, 306–312. (doi:10.1038/hdy.2012.43)
Sanada-Morimura S, Matsumura M, Noda H. 2013
Male killing caused by a Spiroplasma symbiont in
the Small Brown Planthopper, Laodelphax
striatellus. J. Hered. 104, 821 –829. (doi:10.1093/
jhered/est052)
Stouthamer R, Luck RF, Hamilton WD. 1990
Antibiotics cause parthenogenetic Trichogramma
(Hymenoptera/Trichogrammatidae) to revert to sex.
Proc. Natl Acad. Sci. USA 87, 2424 –2427. (doi:10.
1073/pnas.87.7.2424)
Russell JE, Stouthamer R. 2011 The genetics and
evolution of obligate reproductive parasitism in
Trichogramma pretiosum infected with
parthenogenesis-inducing Wolbachia. Heredity 106,
58 –67. (doi:10.1038/hdy.2010.48)
Kraaijeveld K, Reumer BM, Mouton L, Kremer N,
Vavre F, Alphen JJM. 2011 Does a parthenogenesisinducing Wolbachia induce vestigial cytoplasmic
incompatibility? Naturwissenschaften 98, 175–180.
(doi:10.1007/s00114-010-0756-x)
Pannebakker BA, Schidlo NS, Boskamp GJF, Dekker
L, Dooren TJM, Beukeboom LW, Zwaan BJ,
Brakefield PM, Alphen JJM. 2005 Sexual
functionality of Leptopilina clavipes (Hymenoptera:
Figitidae) after reversing Wolbachia-induced
parthenogenesis. J. Evol. Biol. 18, 1019–1028.
(doi:10.1111/j.1420-9101.2005.00898.x)
Negri I, Pellecchia M, Mazzoglio PJ, Patetta A, Alma
A. 2006 Feminizing Wolbachia in Zyginidia pullula
(Insecta, Hemiptera), a leafhopper with an XX/X0
sex-determination system. Proc. R. Soc. B 273,
2409 –2416. (doi:10.1098/rspb.2006.3592)
Bouchon D, Cordaux R, Grève P. 2009 Feminizing
Wolbachia and the evolution of sex determination in
rstb.royalsocietypublishing.org
18. Ross L, Pen I, Shuker DM. 2010 Genomic conflict in
scale insects: the causes and consequences of
bizarre genetic systems. Biol. Rev. 85, 807 –828.
(doi:10.1111/j.1469-185X.2010.00127.x)
19. Brown SW, Nelson-Rees WA. 1961 Radiation analysis
of a lecanoid genetic system. Genetics 46, 983.
20. Kitchin RM. 1970 A radiation analysis of a
comstockiella chromosome system: destruction of
heterochromatic chromosomes during
spermatogenesis in Parlatoria oleae (Coccoidea:
Diaspididae). Chromosoma 31, 165 –197. (doi:10.
1007/BF00285146)
21. Brown SW. 1964 Automatic frequency response in
the evolution of male haploidy and other coccid
chromosome systems. Genetics 49, 797.
22. Hartl DL, Brown SW. 1970 The origin of male
haploid genetic systems and their expected sex
ratio. Theor. Popul. Biol. 1, 165–190. (doi:10.1016/
0040-5809(70)90033-X)
23. Borgia G. 1980 Evolution of haplodiploidy: models
for inbred and outbred systems. Theor. Popul. Biol.
17, 103 –128. (doi:10.1016/0040-5809(80)90001-5)
24. Haig D. 1993 The evolution of unusual
chromosomal systems in coccoids: extraordinary sex
ratios revisited. J. Evol. Biol. 6, 69– 77. (doi:10.
1046/j.1420-9101.1993.6010069.x)
25. Haig D. 1993 The evolution of unusual
chromosomal systems in sciarid flies: intragenomic
conflict and the sex raio. J. Evol. Biol. 6, 249–261.
(doi:10.1046/j.1420-9101.1993.6020249.x)
26. Herrick G, Seger J. 1999 Imprinting and paternal
genome elimination in insects. In Genomic
imprinting: an interdisciplinary approach, vol. 25
(ed. R Ohlsson), pp. 41 –71. Berlin, Germany:
Springer.
27. Úbeda F, Normark BB. 2006 Male killers and the
origins of paternal genome elimination. Theor.
Popul. Biol. 70, 511–526. (doi:10.1016/j.tpb.2006.
06.011)
28. Normark BB. 2004 Haplodiploidy as an outcome of
coevolution between male-killing cytoplasmic
elements and their hosts. Evolution 58, 790 –798.
(doi:10.1111/j.0014-3820.2004.tb00412.x)
29. Normark BB. 2006 Perspective: maternal kin groups
and the evolution of asymmetric genetic systems:
genomic imprinting, haplodiploidy, thelytoky.
Evolution 60, 631–642. (doi:10.1111/j.0014-3820.
2006.tb01145.x)
30. Haig D. 2004 Genomic imprinting and kinship: how
good is the evidence? Annu. Rev. Genet. 38, 553–
585. (doi:10.1146/annurev.genet.37.110801.142741)
31. Moran NA, McCutcheon JP, Nakabachi A. 2008
Genomics and evolution of heritable bacterial
symbionts. Annu. Rev. Genet. 42, 165 –190.
(doi:10.1146/annurev.genet.41.110306.130119)
32. Saumitou-Laprade P, Cuguen J, Vernet P. 1994
Cytoplasmic male sterility in plants: molecular
evidence and the nucleocytoplasmic conflict. Trends
Ecol. Evol. 9, 431– 435. (doi:10.1016/01695347(94)90126-0)
33. Werren JH, Baldo L, Clark ME. 2008 Wolbachia:
master manipulators of invertebrate biology. Nat.
Downloaded from http://rstb.royalsocietypublishing.org/ on May 10, 2017
74.
75.
76.
77.
78.
biogeography of Symbiodinium. Annu. Rev. Ecol.
Syst. 34, 661–689. (doi:10.1146/annurev.ecolsys.
34.011802.132417)
Taylor MW, Radax R, Steger D, Wagner M. 2007
Sponge-associated microorganisms: evolution, ecology,
and biotechnological potential. Microbiol. Mol. Biol.
Rev. 71, 295–347. (doi:10.1128/MMBR.00040-06)
Dubilier N, Bergin C, Lott C. 2008 Symbiotic
diversity in marine animals: the art of harnessing
chemosynthesis. Nat. Rev. Microbiol. 6, 725– 740.
(doi:10.1038/nrmicro1992)
Weeks AR, Velten R, Stouthamer R. 2003 Incidence
of a new sex-ratio-distorting endosymbiotic
bacterium among arthropods. Proc. R. Soc. Lond. B
270, 1857– 1865. (doi:10.1098/rspb.2003.2425)
Haig D. 1992 Brood reduction in gymnosperms. In
Cannibalism: ecology and evolution among diverse
taxa (eds M Elgar, B Crespi), pp. 63 –84. Oxford,
UK: Oxford University Press.
Haig D. 2000 The kinship theory of genomic
imprinting. Annu. Rev. Ecol. Syst. 31, 9– 32. (doi:10.
1146/annurev.ecolsys.31.1.9)
10
Phil. Trans. R. Soc. B 369: 20130364
68. Nielsen EE, Hemmer-Hansen J, Larsen PF, Bekkevold
D. 2009 Population genomics of marine fishes:
identifying adaptive variation in space and time.
Mol. Ecol. 18, 3128 –3150. (doi:10.1111/j.1365294X.2009.04272.x)
69. Weersing K, Toonen RJ. 2009 Population genetics,
larval dispersal, and connectivity in marine systems.
Mar. Ecol. Prog. Ser. 393, 1–12. (doi:10.3354/
meps08287)
70. Suttle CA. 2005 Viruses in the sea. Nature 437,
356 –361. (doi:10.1038/nature04160)
71. Hamilton WD, Axelrod R, Tanese R. 1990
Sexual reproduction as an adaptation to
resist parasites (a review). Proc. Natl Acad.
Sci. USA 87, 3566– 3573. (doi:10.1073/pnas.87.
9.3566)
72. Mostowy R, Engelstadter J. 2012 Host–parasite
coevolution induces selection for conditiondependent sex. J. Evol. Biol. 25, 2033–2046.
(doi:10.1111/j.1420-9101.2012.02584.x)
73. Baker AC. 2003 Flexibility and specificity in coral–
algal symbiosis: diversity, ecology, and
rstb.royalsocietypublishing.org
63. Hamilton WD. 1978 Evolution and diversity under
bark. In Diversity of insect faunas (eds LA Mound,
N Waloff ), pp. 154 –175. Oxford, UK: Blackwell
Scientific.
64. Hamilton WD. 1993 Inbreeding in Egypt and in this
book: a childish perspective. In The natural history
of inbreeding and outbreeding: theoretical and
empirical perspectives (ed. NW Thornhill), pp. 429–
450. Chicago, IL: The University of Chicago Press.
65. Engelstädter J, Hurst GDD. 2006 Can maternally
transmitted endosymbionts facilitate the evolution
of haplodiploidy? J. Evol. Biol. 19, 194–202.
(doi:10.1111/j.1420-9101.2005.00974.x)
66. Ross L, Shuker DM, Normark BB, Pen I. 2012
The role of endosymbionts in the evolution of
haploid-male genetic systems in scale insects
(Coccoidea). Ecol. Evol. 2, 1071 –1081. (doi:10.
1002/ece3.222)
67. Wilkins JF, Haig D. 2003 What good is genomic
imprinting: the function of parent-specific gene
expression. Nat. Rev. Genet. 4, 359 –368. (doi:10.
1038/nrg1062)