Biological Journal of the Linnean Society (1987), 32: 385-393
Symbiont-induced speciation
JOHN N. THOMPSON
Departments of Botany and <oolog~, Washington State University, Pullman, WA 99164,
U.S.A.
Received 16 March 1987, accepted f o r publication 20 Jub 1987
Speciation induced by parasitic or mutualistic symbionts has been suggested for taxa ranging from
plants to insects to monkeys. Previous models for symbiont-induced speciation have been based
upon hybrid inferiority and selection for reinforcement genes. Taken on their own, however, such
models have severe theoretical limitations and little empirical support. Two conditions that may
favour symbiont-induced speciation are presented here: (1) interaction norms in which the
outcomes of hostlsymbiont interactions differ between environments and (2) differential
coadaptation of host and symbiont populations between environments or along an environmental
gradient. Symbiont-induced speciation can be considered as one form of ‘mixed-process
coevolution’: reciprocal evolution in which adaptation of a population of one species to a
population of a second species (or coadaptation of the populations) causes the population of the
second species to become reproductively isolated from other populations.
KEY WORDS: Coevolution
~
interaction norms
-
mutualism
~
parasitism
-
speciation.
CONTENTS
Introduction . . . . . . . . . . . . .
Suggested cases of symbiont-induced speciation . . . . .
Suggested mechanisms: hybrid inferiority and reinforcement genes
. . . . . .
Inadequacy of the suggested hypotheses
Interaction norms and coadaptation
. . . . . . .
Acknowledgements
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References. . . . . . . . . . . . . .
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INTRODUCTION
The possibility that coevolution between species can lead directly to speciation
has long been an attractive idea (Gillett, 1962; Bock, 1972, 1979; Thompson,
1982; Kiester, Lande & Schemske, 1984). As two or more interacting species
undergo coevolution (reciprocal evolutionary change), the genetic changes may
result in divergence and reproductive isolation between populations of at least
one of the species. Variations on this general idea have been used repeatedly to
suggest how reproductive isolation developed between pairs of species (Table 1).
The ecological and genetic conditions under which such interspecific
interactions are likely to lead directly to speciation, either with or without
coevolution, remain largely unanalysed. In this paper I first review the
suggested cases of coevolution-induced speciation between symbionts and hosts,
then consider the suggested mechanisms of speciation, and then finally suggest a
0024-4066/87/120385
+ 09 $03.00/0
385
0 1987 The Linnean
Society of London
Horizontal
Wolbachia sp.
Rickettsia
Unidentified
Plasmodium
Plasmodium
Gregarine protozoan
Ephestia cautella moths
Hypera postica weevils
Tribolium confusion beetles
Anopheles spp. mosquitoes
Maccaca mulatta and M . fascicularis
macaques
Haploembia solieri
Antagonism to ?
Antagonism to ?
Antagonism to ?
Antagonism to commensalism
Antagonism to near
commensalism
Antagonism
Antagonism to ?
Antagonism to ?
Antagonism to mutualism
Antagonism to mutualism
Range of outcome
~
Shown
Shown
Shown
Assumed
Assumed
Shown
Shown
Shown
Shown
Hybrid
inferiority*
~
Stefani (1956, 1960), White (1978)
Dobzhansky et al. (1976), Ehrman
(1983), Somerson et al. (1984)
Powell (1982)
Hoffman et 01. (1986)
Yen & Barr (1971, 1973), Barr
(1980), Awahmukalah & Brooks
( 1985)
Kellen & Hoffman (1981)
Hsiao & Hsiao (1985)
Wade & Stevens (1984)
Steiner (1981)
Wheatley (1980)
Reference
*Hybrid inferiority ranges tiom failure of embryonic development in hybrid zygotes to reduced viability or fertility in hybrid adults.
~~
Vertical
Vertical
Vertical
Horizontal
Horizontal
Unidentified
Unidentified
Wolbachia pipientis
Drosophila pseudoobscura
Drosophila simulans
Culux pipiens complex mosquitoes
~~
Vertical
M ycoplasma-like
Drosophila paulistorum
Vertical
Vertical
Vertical
Mode of
transmission
Symbiont
Hosts
Table 1 . Taxa in which microbial symbionts (parasitic or mutualistic) have been proposed as the direct cause of
reproductive isolation between host populations or as the major cause of selection resulting in speciation
P2
3:
el
7
+
COEVOLUTION AND SPECIATION
387
set of ecological conditions that could potentially lead to speciation. ‘Symbiont’
is used here in its general sense of a species that lives in intimate and usually lifelong association with another species; the interaction may be antagonistic,
commensalistic, or mutualistic. This paper focuses on interactions between
symbionts and hosts, because these kinds of interactions have been most
commonly implicated as direct causes of speciation.
SUGGESTED CASES OF SYMBIONT-INDUCED SPECIATION
The studies listed in Table 1 have suggested several kinds of symbiont
involvement in host speciation: ( 1) a maternally-inherited symbiont directly
causes reduced viability or fecundity in male hybrids between host populations,
and speciation may result from such hybrid inferiority (Powell, 1982); (2) a
horizontally transmitted parasite has a more detrimental effect on some host
genotypes than on others and selection favours assortative mating among those
genotypes (Wheatley, 1980; Steiner, 1981); or (3) a parasite causes sterility in
males in some populations and favours the evolution of parthenogenetic sibling
species (Stefani, 1956, 1960; White, 1978).
The examples considered here involve protozoans, bacteria, rickettsias, or
potentially smaller sequences of DNA or RNA that are symbionts within hosts.
Other kinds of interactions have been implicated in speciation (Ehrlich &
Raven, 1964; Bock, 1972, 1979; Thompson, 1982; Kiester et al., 1984), but
symbionts have been suggested most commonly as direct and immediate causes
of initial divergence and reproductive isolation in host populations. In some
potential cases of symbiont-induced reproductive isolation, it would be difficult
to call a species the relatively small sequences of DNA or RNA that act as the
symbiont, as for example in interactions between a virus and its host. But these
are problems only in terminology and its limits. The vertical or horizontal
transmission of extranuclear genetic material with different kinds of genetic
organization will ultimately allow a comparison of how the structure of genomes
affects the genetics of coevolution.
The examples differ in the mode of transmission of the symbiont. I n some
cases, such as the mycoplasma-like symbionts in Drosophila paulistorum or the
rickettsiae in Tribolium confusum, the symbiont is transmitted vertically from
females to their offspring. Such germ-line transmission is known to occur in a
wide variety of micro-organisms (Grun, 1976; Mims, 1981), and has the
potential to be involved in the evolution of reproductive isolation in many host
taxa. I n other suggested cases, such as with Plasmodium and the gregarine
protozoan that attacks Haploembia solieri, the symbiont is transmitted
horizontally among individuals rather than from females to offspring.
The suggested cases involve symbionts that range from antagonism to
mutualism in their effects on host fitness. For example, species in the D. paulistorum group differ in the mycoplasma-like symbionts that they harbour,
and these symbionts appear to be mutualistic only with their specific host
populations (Ehrman, 1983). So this example involves a symbiont that can be
antagonistic or mutualistic depending upon its genotype and that of the host. I n
contrast, other examples, including the suggested cases of Plasmodium-induced
speciation in macaques (Wheatley, 1980) and mosquitoes (Steiner, 1981),
involve symbionts that range from parasitic to almost commensalistic,
388
J. N. THOMPSON
depending partly upon the genotypes in the host population. In still other cases,
it is unknown whether the symbionts are commensalistic or mutualistic with
their host populations, but the symbionts cause lowered viability or fecundity in
hybrids between the host populations (Wade & Stevens, 1984). Hence, the
suggested cases of symbiont-induced speciation in hosts include a variety of
micro-organisms that differ in their mode of transmission and range of outcomes
in host populations.
SUGGESTED MECHANISMS: HYBRID INFERIORITY AND REINFORCEMEN'I' GENES
Few specific mechanisms for symbiont-induced speciation have been
examined, but most suggested hypotheses have relied upon hybrid inferiority
and selection for genes that promote pre-mating isolating barriers
(reinforcement genes). That is, post-mating isolating barriers are expected to
lead eventually to pre-mating isolating barriers through selection against
genotypes that mate with individuals from other populations. Selection for
reinforcement genes, for example, was the basis of the experimental attempts to
produce reproductive isolation between populations of D. paulistorum
(Dobzhansky, Pavlovsky & Powell, 1976), which may differ in the mycoplasmalike symbionts they harbour (Ehrman & Kernaghan, 1971; Ehrman, 1983). In
these experiments, the systematic elimination of hybrids resulted in an increase
in homogamic matings over the course of 131 generations of selection, but
complete pre-mating reproductive isolation was not achieved.
Another variation of the hybrid inferiority/reinforcement hypothesis was
suggested by Steiner (1981) for speciation in Anopheles mosquitoes. There is
variation among sibling species complexes of Anopheles in the extent to which
physiology, survival or reproduction of individuals is affected by malarial
parasites. Using a verbal genetic model with one polyallelic locus, Steiner
envisioned three host alleles with different effects: a parasite-compatible allele,
which allows Plasmodium to be carried within the mosquito with little or no effect
on mosquito fitness; a parasite-sensitive allele, which results in reduced fitness in
individuals carrying Plasmodium; and a recessive parasite-resistant allele, which
when homozygous makes the mosquitoes resistant to carrying Plasmodium. The
behaviour of most heterozygotes was unspecified in the model but hybrid
inferiority was assumed. Steiner argued that these conditions allow for
speciation through either disruptive selection on the parasite-compatible and
parasite-resistant genotypes, or a shift of individuals with the parasite-sensitive
alleles onto a new host or into a new habitat in which the chance of infection
with Plasmodium is low.
In some cases, hybrid inferiority is expressed as hybrid-male sterility caused
by cytoplasmic incompatibility: hybridization between populations produces
offspring in which females are fertile, but males are sterile due to incompatibility
between the cytoplasm from the one population and a nuclear gene from the
other population. Such incompatibility can involve any of a variety of cell
organelles or symbionts transmitted vertically through maternal cytoplasm
(Grun, 1976; Wade & Stevens, 1984; Ehrman & Powell, 1982; Hsiao & Hsiao,
1985; Hoffman, Turelli & Simmons, 1986). Hybrid male sterility through
cytoplasmic incompatibility has been suggested as a route to speciation
(Caspari, 1948; Jones, 1951; Laven, 1958; Grun & Aubertin, 1965; Somerson,
COEVOLUTION AND SPECIATION
389
Ehrman, Kocka & Gottlieb, 1984), and Powell (1982) argued that symbionts
could cause host speciation in this way with little or no genetic change in the
host population.
Yet another variation on the process of symbiont-induced speciation was
suggested for the web-spinner Haploemia solieri (Stefani, 1956, 1960; White,
1978): a horizontally transmitted parasite that renders males sterile may favour
the evolution of parthenogenetic sibling species of the host. The H. solieri
complex is a group of bisexual and parthenogenetic populations that may be
sibling species. Males, but not females, of the bisexual populations are often
made sterile because of parasitism by a gregarine protozoan, and Stefani (1956,
1960) found a positive correlation between the percentage of individuals
parasitized and the proportion of parthenogenetic females within populations.
White (1978) argued that is is therefore conceivable that the evolution of
parthenogenetic females has been favoured in populations with high rates of
parasitism.
INADEQUACY OF THE SUGGESTED HYPOTHESES
The major problem with the above speciation hypotheses is that most rely
upon hybrid inferiority and selection for reinforcement genes. Both theoretical
models and experimental analyses have indicated that speciation relying upon
this mechanism alone requires a fairly low initial number of errors in mating,
strong selection, and population levels that are maintained independently
through the generations of selection (Templeton, 1981). I n the absence of these
conditions, it is more likely that either one of the host populations will become
extinct or the populations will fuse as the alleles causing hybrid inferiority are
lost through selection (Paterson, 1978; Templeton, 1981).
How often the restrictive conditions allowing reinforcement are met in
natural populations, is of course unknown. It seems unlikely, however, that they
are common. Selection favouring reinforcement is probably weaker in most
cases than selection favouring modifiers that decrease hybrid inferiority.
Selection for reinforcement can operate only indirectly through the association
between alleles at loci affecting assortative mating and those a t loci affecting
hybrid inferiority. So it is likely to be less effective than selection acting directly
on modifiers that decrease hybrid inferiority (Barton & Hewitt, 1985; Butlin,
1987). Moreover, recent reviews of hybrid or potential hybrid zones between
populations have revealed few cases providing evidence of reinforcement
(Barton & Hewitt, 1985; Butlin, 1987). Consequently, the evolution of
reinforcement genes via hybrid inferiority alone may not generally be a likely
route to symbiont-induced speciation.
The specific problem of male sterility in hybrids, which is sometimes
associated with maternally-inherited symbionts (Wade & Stevens, 1984;
Ehrman & Powell, 1982; Hsiao & Hsiao, 1985), has been studied in detail for
cases involving cytoplasmic incompatibility due to a single nuclear gene. These
studies have shown that speciation is unlikely if the incompatibility is due only
to a single recessive nuclear gene: selection will tend to eliminate the gene that
results in male sterility and the populations will fuse (Watson & Caspari, 1960;
Caspari, Watson & Smith, 1966; Constantino, 1971). These theoretical studies,
however, make two important assumptions: the nuclear gene is not adaptive in
390
J . N. THOMPSON
any other way, and the outcome of the interaction between the symbiont and
host does not vary between host populations. Relaxation of these assumptions
provides a potential route to symbiont-induced speciation, and the consequences
are explored in the following section.
INTERACTION NORMS AND COADAPTATION
Theoretical studies of population differentiation along environmental
gradients or between habitats have shown that genetic differentiation is possible
even in the presence of some gene flow between populations (Slatkin, 1973,
1985; Endler, 1977; Barton & Charlesworth, 1984). I n fact, the evolution of
reproductive isolation along a cline may not demand reinforcement genes,
which are required in most models of reproductive isolation in the absence of
environmental gradient or major differences between habitats (Templeton,
1981). Using these results it is possible to construct an hypothesis for symbiontinduced speciation that involves two components: a n interaction norm that
varies across an environmental gradient or between habitats, and differential
coadaptation between symbionts and hosts across environments. An interaction
norm can be defined as the range of variation in outcome of interactions across
different environments as genotypes are held constant (Thompson, 1986a, b).
The term is in parallel to reaction norm as used in population genetics to mean
the array of phenotypes expressed by a genotype across a series of environments
(Schmalhausen, 1949; Lewontin, 1974; Gupta & Lewontin, 1982; Parker,
1985).
The outcomes of interactions can vary broadly across environments. I n some
cases, a n interaction that is antagonistic in one environment may be
commensalistic or mutualistic in another environment (Roughgarden, 1975,
1983; Thompson, 1982; Levin & Lenski, 1983). Outcomes that range from
antagonism to mutualism are in fact known from a variety of interactions
between symbionts and related host populations or species (Dobzhansky et al.,
1976; Grun, 1976; Jeon & Jeon, 1976; Margulis, 1981, 1984). Some interactions,
for example, appear to be mutualistic primarily under environmental conditions
that impose nutrient stress (Yonge, 1968; Lewis, 1973; Janzen, 1974; Huxley,
1980; Janos, 1980; Thompson, 1981, 1982; Holl, 1983). Mycorrhizal
relationships are often mutualistic in infertile soils but can be antagonistic in
more fertile soils, causing a depression in growth rate of the host plant (Bowen,
1980). Other interactions are similar in their general outcome across
environmental gradients (antagonism, commensalism, or mutualism), but may
differ in the specific host genotypes that are favoured in different environments
(Gilbert, 1983; Thompson, 1985).
Consequently, as the outcome of an interaction varies along an environmental
gradient or between habitats, selection could favour different host and symbiont
alleles. The process of coadaptation could even involve different loci in the
different environments. For example, alleles increasing the probability of
interaction may be favoured in environments where the interaction is
mutualistic, while alleles decreasing the probability of interaction may be
favoured in the host in environments in which the interaction is antagonistic. It
is possible, then, to conceive of different habitats or environmental gradients
along which the outcome of the interaction varies through differences in the
phenotypic expression of genes. These differences in the outcome of the
COEVOLUTION AND SPECIATION
39 1
interaction could then lead to population divergence as different alleles are
favoured in different environments. If gene flow is fairly low between
populations, coadaptation could proceed in very different directions in different
populations, and involve different sets of genes in different environments.
The interaction norm perhaps most likely to generate differential
coadaptation in different habitats or along a n environmental gradient would be
one that ranged from antagonism to mutualism. The process could also work if
the interaction were antagonistic or mutualistic across all environments, but the
specific effects of the interaction on the host varied among environments. For
example, host populations could occur across a range of environments, all of
which are nutrient-poor or toxin-rich but for different ratios of nutrients or
toxins. A mutualistic symbiont could contribute to host nutrition or degredation
of toxins in all populations, but the host and symbiont genes involved in the
mutualism could differ significantly between the host populations.
Consequently, variation in the outcome of interactions among environments
could potentially lead to reproductive isolation partly as a pleiotropic outcome
of differential coadaptation. This is in contrast to other suggested hypotheses for
symbiont-induced speciation, which rely mostly on hybrid inferiority alone as
the initial cause of speciation. If there were no differential selection on the
symbiont/host interaction among environments, then selection could potentially
act to eliminate hybrid inferiority. The imposition, however, of differences
among environments in selection on the interaction would continue over time to
increase differences among the populations. Differential coadaptation of
symbiont and host populations among environments could quickly multiply the
number of causes of hybrid inferiority over time and make it less likely that such
inferiority could be eliminated. Hence, elimination of hybrid inferiority between
host populations would no longer be simply a result of elimination of a few
particular alleles depressing hybrid fitness. I t is this differential selection among
environments on the symbiont/host interaction that could continue to magnify
the differences among the populations and makes this suggested mechanism
different from previous hypotheses on the mechanisms of symbiont-induced
speciation.
Identifying specific ways in which coevolution involves adaptation and
speciation is crucial to the development of an understanding of the conditions
that favour different forms of coevolutionary change. Coadaptation,
cospeciation and the Ehrlich & Raven (1964) hypothesis are three of the
proposed forms. Symbiont-induced speciation can be considered as one form of
‘mixed-process coevolution’: reciprocal evolution of interacting species in which
adaptation of a population of one species to a population of a second species (or
coadaptation of the populations) causes the population of the second species to
become reproductively isolated from other populations (Thompson, 1986a). By
identifying different forms of coevolution and the conditions under which they
are likely to occur, it will be possible to develop a richer theory of coevolution
that shows the variety of routes of coevolutionary change.
ACKNOWLEDGMENTS
I thank M. J. Crawley, J. A. Endler, W. D. Hamilton, I. Hanski, M. P.
Hassell, A. D. Taylor, and J. K. Waage and an anonymous reviewer for
discussions or helpful comments on the manuscript. I am grateful to the
392
J. N. THOMPSON
Department of Pure and Applied Biology, Imperial College (Silwood Park) for
the use of its facilities while I was writing the manuscript. This work was
supported in part by USDA Competitive Grant (Biological Stress) 84-CRCR- 11395.
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