Behavioral Ecology Vol. 10 No. 3: 333-337
© 1999 International Society for Behavioral Ecology
Forum |
The beneficial sexually transmitted microbe hypothesis of avian copulation
a Department of Biology, Grand Valley State University, Allendale, MI 49401-9403, USA b Department of Ecology, Evolution and Natural Resources, 80 Nichol Avenue, Rutgers University, New Brunswick, NJ 08901-2882, USA
Received 3 September 1997; first revision 7 April 1998; second revision 28 September 1998; accepted 28 August 1998.
ABSTRACT
Several hypotheses have been proposed to explain why female birds either copulate repeatedly with a single mate or copulate with multiple partners even though only a single copulation may be sufficient to fertilize an entire clutch. We hypothesize that females may directly benefit from high frequencies of copulation and multiple copulation partners if they receive a cloacal inoculation of beneficial sexually transmitted microbes (STMs) that can either protect them against future encounters with pathogens and/or serve as therapy against present infections. Experiments in domestic animal production, wildlife rehabilitation, and clinical medicine indicate that inoculations of beneficial microbes derived from the indigenous microflora of hosts can lead to nutritional benefits, resistance to colonization by pathogens, the elimination of infection, and improved immune system functioning in recipients. Our hypothesis predicts greater copulatory rates when the probability of the transmission of beneficial microbes exceeds that of pathogens and when the positive effects of beneficial microbes on host fitness exceed the negative effects of pathogens. Patterns of copulatory behavior in birds suggest the potential utility of our hypothesis. We discuss our hypothesis in the context of observed patterns of copulation in birds and propose some ways to directly test our hypothesis. Information on the probabilities of transmission during copulation of beneficial and pathogenic microbes and their relative potencies in birds are needed to directly test the predictions of our hypothesis.
Key words: beneficial microbes, birds, copulations, extrapair copulations, sexually transmitted diseases, sexually transmitted microbes.
A plethora of hypotheses (e.g., Birkhead
and Møller, 1992
;
Birkhead et al., 1987;
Hunter et al., 1993;
Keller and Reeve, 1995;
Lumpkin, 1981;
Petrie, 1992) have been
proposed to explain the variations in copulatory behavior both among and
within species of birds (Birkhead et al.,
1987). Despite a great deal of theoretical musing over the
potential costs and benefits of copulations to females, including extrapair
copulations (EPCs), the realized costs and benefits are not very clear (e.g.,
Birkhead and Møller,
1992; Birkhead et al.,
1990; Hamilton,
1990; Kempenaers et al.,
1992; Lifjeld et al.,
1993; Møller,
1994; Wagner,
1991, 1992;
Westneat et al., 1990). Direct
empirical evidence supporting or contradicting any hypothesized benefit to
females is lacking for most species.
We propose that the cloacal inoculation of beneficial sexually transmitted
microbes (STMs; viruses, bacteria, fungi) is a previously ignored direct
benefit to females of participating in copulations. Our hypothesis explains
why female birds might pursue multiple copulations with their mates or EPCs
with males of higher quality than their social mates, and is at least as
parsimonious as theories that predict only indirect female benefits (e.g.,
"good genes"; Hamilton and
Zuk, 1982, see below). Although our hypothesis is directed at
birds, it may also apply to other animals.
The avian cloaca serves the dual functions of excretion and gamete
transfer. Microbes may be readily transmitted from males to females during
copulation because intestinal microbes could become incorporated into an
ejaculate (Sheldon, 1993).
Thus, sexually transmitted diseases (STDs) may be important selective forces
in the evolution of avian mate choice
(Hamilton, 1990) and mating
systems (Lombardo, 1998;
Sheldon, 1993). But microbes
can also have beneficial effects on host health
(Herceg and Peterson, 1997;
Hutchenson et al., 1991;
Prescott et al., 1996;
Savage, 1977;
van der Waaij, 1989) and
therefore on reproductive success. The benefits associated with the horizontal
transmission of beneficial microbes may be a selective force helping to mold
the evolution of mate choice and copulation behavior in birds.
A theory that posits that female birds seek multiple copulations with one or more partners in order to be inoculated with beneficial microbes must meet these requirements: (1) microbes can have beneficial effects, (2) birds transmit beneficial microbes during copulation, (3) the transmitted microbes produce beneficial effects in their recipients, and (4) the probability of transmission and potency of effect of beneficial microbes relative to that of potential pathogens influences copulatory behavior.
Requirement 1: the beneficial effects of microbes
Studies in commercial animal husbandry, wildlife rehabilitation, and
clinical medicine demonstrate the beneficial effects of microbes on their
hosts. The beneficial effects of gastrointestinal microbes are well documented
in commercial animal husbandry (for reviews see
Fuller, 1989;
Hutchenson et al., 1991).
Newborn and juvenile domestic animals inoculated with beneficial microbes are,
on average, less likely to harbor potentially pathogenic species, grow more
rapidly, and better resist challenges by pathogens than are uninoculated
individuals (Hutchenson et al.,
1991).
The beneficial effects of microbes in wild birds is suggested by the use of
adult saliva during the rehabilitation of chimney swifts (Chaetura
pelagica; Kyle and Kyle,
1993). The adult saliva contained a variety of microbes. The
saliva used in rehabilitation could come from any healthy adult swift. Nearly
100% of nestling swifts less than 6 days old died if given food lacking the
adult saliva supplement, whereas nearly 100% of those fed food inoculated with
saliva were rehabilitated and released
(Kyle and Kyle, 1993).
Beneficial microbes have also been used as therapy against infection (e.g.,
Bruce and Reid, 1988;
Gorbach et al., 1987). In
humans, crude fecal suspensions obtained from healthy individuals and
administered as enemas to sick individuals have been used effectively to treat
enterocolitis caused by Clostridium difficile
(Bowden et al., 1981;
Schwann et al., 1984). In
rhesus monkeys (Macca maculata), vaginal Escherichia coli
infections have been cured by treatment with direct intravaginal application
of vaginal microbes obtained from healthy monkeys
(Herthelius et al., 1989).
Many studies have demonstrated that (1) "normal" indigenous
microbes are important in providing resistance to intestinal pathogens and
controlling the populations of opportunistic bacteria in the digestive and
urogenital tracts in humans (e.g., Agnew
and Hillier, 1995; Bruce and
Reid, 1988; Hillier and
Holmes, 1990; Lidbeck and
Nord, 1993; Redondo-Lopez et
al., 1990; Savage,
1977; Sobel, 1990;
van der Waaij et al., 1971),
other mammals (Savage, 1969),
and birds (Fuller, 1973,
1989;
Hutcheson et al., 1991;
Nurmi and Rantala, 1973;
Snoeyenbos et al., 1983;
Weinack et al., 1981,
1982), and (2) there is a host
genetic component to the development of the indigenous microflora
(Stern et al., 1990;
van der Waaij, 1989;
van der Waaij et al.,
1971).
Mechanisms by which females may receive therapeutic inoculations include
(1) bacteriophagic viruses (e.g., Levin
and Bull, 1996; Smith and
Huggins, 1983), (2) less virulent strains of pathogens, which, in
becoming established, limit the colonization abilities of more virulent
strains (Sprunt and Leidy,
1988), and (3) beneficial microbes that produce bacteriocins
lethal to already resident pathogenic strains
(Daw and Falkiner, 1996;
Jack et al., 1991;
Waters and Crosa, 1991).
The microbial population of a healthy individual consists of a mixture of
beneficial and potentially pathogenic microbes that can cause illness and
death if the balance between them is disrupted
(Fuller, 1989;
Herceg and Peterson, 1997;
Prescott et al., 1996;
Savage, 1977;
van der Waaij, 1989). Physical
and psychological stress can disrupt the protective microflora
(Tannock, 1983), leading to
increases in pathogen populations and subsequent pathology
(Fuller, 1989). One general
effect of stress is for protective Lactobacilli spp. to decrease and
pathogenic coliforms to increase (Fuller,
1989; Tannock,
1983). In addition, the hormonal state arising from changes in
diet (Scrimshaw et al., 1968)
and reproductive condition may affect the ability of the immune system to
combat pathogens (Folstad and Karter,
1992). Thus, for many birds it is likely that the rigors of
migration, territory establishment and defense, ecological and sexual
competition, and reproduction itself influence the ecological balance of the
microbes of the gastrointestinal and urogential tracts, making them more
susceptible to pathogens (Tannock,
1983).
Reproduction may be especially stressful. For example, infections of the
blood parasite Haemoproteus spp. and heterophile:lymphocyte ratios
which indicate stress in birds were positively correlated with reproductive
effort in great tits (Parus major,
Ots and Horak, 1996). The fact
that the ecological balance between microbes in the gastrointestinal and
urogenital tracts can be disrupted by situations that are commonly encountered
by wild birds establishes the conditions necessary for our hypothesis.
For adult birds, potential pathways for the acquisition of beneficial
microbes include copulation, mate feeding, coprophagy (cf.
Troyer, 1982), and/or
cloaca-pecking (cf. Davies,
1983). Coprophagy may be an inefficient way to obtain beneficial
microbes that are obligate anaerobes (e.g., most Lactobacilli spp.)
(Topley, 1983;
Bokkenheuser, 1993), favoring
the evolution of direct interindividual transmission by copulation or
mouth-to-mouth transfer. The most direct pathway would be via copulation
because it minimizes the exposure of gastrointestinal and urogential microbes
to hostile aerobic environments.
Requirements 2 and 3: the sexual transmission of microbes and their effects
The existence of avian STDs (Lockhart
et al., 1996; Sheldon,
1993; Stipkovits et al.,
1986) is direct evidence that birds inoculate each other with
microbes during copulation. Moreover, Perek et al.
(1969) showed by experiment
that male domestic cockerels with semen contaminated with bacteria infected
the females with which they copulated.
For females to benefit from receiving cloacal inoculations of beneficial
microbes, those microbes must become established in the gastrointestinal
and/or urogenital tract. Corrier et al.
(1991) showed that cloacal
inoculation of turkey poults with beneficial microbes reduced the load of
gastrointestinal Salmonella seftenberg after an oral challenge at 3
days of age. This finding shows that microbes introduced into the cloaca can
become established in the gastrointestinal tract and may outcompete pathogens
already resident in the host. In birds, beneficial STMs introduced into the
cloaca have a direct route into the intestines and urogential system.
Requirement 4: copulatory behavior in relation to the benefits and risks of sexual transmission of microbes
Explanations for the adaptive significance of variation in copulatory
behavior among different species (Birkhead
et al., 1987), populations (e.g., synchronous versus asynchronous
breeders) (Stutchbury and Morton,
1995), ecological communities (e.g., temperate versus tropical
zones) (Stutchbury and Morton,
1995), and degrees of sociality
(Møller and Birkhead,
1993) in birds have been proposed. However, none has directly
considered the influence that STMs might have on copulatory behavior.
Female attempts to receive beneficial microbes may help explain why some
female birds copulate outside of their fertile periods (e.g.,
Fitch and Shugart, 1984;
Flood, 1985;
Lombardo, 1986;
Power and Doner, 1980;
Quay, 1985,
1989;
Wagner, 1991;
Wolf, 1975). Moreover, it has
been difficult to understand why many female birds copulate repeatedly with
the same male or with multiple males
(Birkhead and Møller,
1992; Hunter et al.,
1993; Petrie,
1992) when only one or few ejaculates may provide enough sperm to
fertilize all of a female's eggs
(Adkins-Regan, 1995;
Birkhead, 1988). Repeated
inoculations of beneficial STMs may be a direct benefit of multiple
copulations and may be necessary for female birds to receive inoculations
large enough to produce benefits. In clinical situations and during domestic
animal production, repeated inoculations of antibiotics and/or beneficial
microbes are used to produce the desired prophylatic, therapeutic, or
nutritional effects (Fuller,
1989; Hutcheson et al.,
1991; Savage,
1969).
The beneficial STM hypothesis of copulation in birds
Our hypothesis is based upon the following assumptions:
- In birds, large numbers of copulations are not necessary to
fertilize all eggs (Adkins-Regan,
1995; Birkhead,
1988). Copulations in excess of the minimum number required for
fertilization require explanation. Part of that explanation is probably that
females seek the benefits of sperm competition
(Birkhead and Møller,
1992; Keller and Reeve,
1995), but we also assume that females can be favored for seeking
any beneficial component of male ejaculate, not just highly
competitive sperm (Eberhard and Cordero,
1995).
- Some birds in the local population carry both beneficial and pathogenic
STMs, while others carry only one or the other, or neither (e.g.,
Brittingham et al., 1988;
Calnek et al., 1991;
Cooper et al., 1980;
Flammer and Drewes, 1988;
Fritz et al., 1992;
Lombardo et al., 1996;
Petrak, 1982). For example, of
30 tree swallow (Tachycineta bicolor) semen samples screened for
microbes in 1998, 11 (37%) were negative, 11 (37%) contained both beneficial
(e.g., Lactobacilli spp.) and potentially pathogenic (e.g.,
Salmonella spp., E. coli) microbes, 1 (3%) contained only
beneficial microbes, and 7 (23%) contained only potentially pathogenic
microbes (Lombardo and Thorpe, unpublished data)
- Beneficial STMs increase the health and vigor of their recipients, enhance
host resistance to pathogenic STMs, and positively affect host reproductive
success; pathogenic STMs have the opposite effects.
- The probability that a female becomes colonized by STMs increases with the
number of copulations she participates in (and/or partners she copulates
with).
- Birds will generally make risk-averting (sensu
Kahneman et al., 1982)
decisions (e.g., avoid partners infected with pathogenic STMs) while pursuing
copulations because this will promote their survival and hence reproductive
success. However, when their probability of survival has already been
compromised by acquisition of pathogenic STMs, birds may be risk seeking
(sensu Kahneman et al., 1982)
to improve their odds of acquiring beneficial STMs as an antidote. Thus, ill
females may increase their number of copulations/partner or number of partners
even though this will inevitably also increase their chances of acquiring
additional pathogenic STMs and thus further decrease their odds for survival
and/or nesting success.
Given these assumptions, we hypothesize that females should pursue copulations to obtain STMs when these conditions obtain: (1) the probability of obtaining beneficial STMs exceeds that of obtaining pathogenic STMs, (2) the positive effects of beneficial STMs are greater than the negative effects of pathogenic STMs, and (3) the opportunity costs of obtaining copulations (i.e, the time, energy, and risk costs) are not too great for the female's budget. Additionally, if increased microbial diversity is beneficial, then mated females should pursue EPCs as well as copulations with their mates. However, the opportunity costs of EPCs will average higher because of mate guarding by the female's own mate, possible attack by the target male's female, and greater average distances between nonmated than mated individuals.
The identification of potential partners
Positive correlations between the presence of beneficial STMs and host
nutrition and resistance to pathogens (i.e., health)
(Fuller, 1989;
Herceg and Peterson, 1997;
Hutcheson et al., 1991;
Prescott et al., 1996;
Savage, 1977;
van der Waaij, 1989) strongly
suggest a similar positive relationship between beneficial microbes and
competitive ability. If carrying beneficial microbes is associated with good
health (Fuller, 1989;
Hutcheson et al., 1991;
Savage, 1977;
van der Waaij, 1989), then the
ability of individuals to identify potential donors of beneficial STMs should
be favored. Furthermore, if individuals that avoid copulating with carriers of
pathogenic STMs have a selective advantage over those that do not, then the
ability to detect infected partners by one sex would favor the ability to
advertise freedom from disease by the other
(Hamilton, 1990). Because
there is a host genetic component to the establishment of symbiotic microbes
(Stern et al., 1990;
van der Waaij, 1989), carriers
of strains of the most beneficial microbes will also simultaneously display
their genetic quality.
An increasing body of empirical evidence suggests that welldeveloped
secondary sexual characters may be reliable signals of health because they may
be positively correlated with superior immunocompetence (sensu
Folstad and Karter, 1992;
Møller and Saino, 1994;
Ros et al., 1997;
Saino et al., 1995,
1997). Likewise,
well-developed secondary sexual characters might also be reliable signals that
an individual carries large numbers of and/or highly potent beneficial
microbes. Therefore, female choice for showy males
(Andersson, 1982;
Møller, 1988;
von Schantz et al., 1989) may
have begun with females choosing the healthiest looking males as mates and EPC
partners because they not only avoided STDs and other infectious diseases, but
also received inoculations of superior beneficial STMs.
Our argument is parallel to the Hamilton and Zuk
(1982) "good
genes" model of female choice, except that in our hypothesis females
receive both direct and indirect benefits from choice. Our hypthesis and good
genes models of choice are complementary, not mutually exclusive. The direct
benefit of avoiding STDs and other infectious diseases by mating with showy
males is implicit in Hamilton and Zuk
(1982). Thus some current
models of parasite-mediated sexual selection
(Clayton, 1991;
Hamilton, 1990;
Hamilton and Zuk, 1982;
Møller, 1994) may be
useful in understanding the dynamics of choice for partners that are likely to
transmit beneficial microbes. Good genes models
(Hamilton and Zuk, 1982) may
be applicable when females pursue copulations during their fertile periods,
although health considerations should always be present. In contrast, if
females pursue copulations outside of their fertile periods (e.g., during
migration; cf. Quay, 1985) or
when their indigenous microflora has been disturbed, then no assumptions about
the genetic quality of potential partners is necessary (cf.
Clayton, 1991), and our
hypothesis is more applicable.
Both partners may be inoculated with STMs during copulation. However,
because most birds lack an intromittant organ and ejaculates move from male to
female, the transmission of microbes during copulation is likely to be
asymmetrical with the probability of transmission from male to female being
greater than that from female to male
(Perek et al., 1969). Thus,
while both sexes are favored for detection and signaling ability, because of
the asymmetry of risk, females would be favored for greater detection ability
and males for greater signaling ability. However, because males should avoid
copulating with females infected with pathogenic STMs, females may be favored
for signaling their freedom from infection (cf.
Hamilton, 1990)
Copulatory behavior in birds and tests of the hypothesis
Directly comparing the predictions of our hypothesis to data on avian
copulatory behavior (see Birkhead et al.,
1987; Birkhead and
Møller, 1992, for reviews) is difficult because
observations of copulation are biased in that they are most often of
within-pair copulations during the breeding season. If females copulate to
achieve fertilization, promote sperm competition, assess potential future
partners, and acquire beneficial STMs, we have no a priori reason to predict
patterns of copulatory behavior different from those already observed.
However, our hypothesis also predicts that females pursue EPCs and copulations
outside of their fertile periods to acquire beneficial STMs. Copulations
performed solely to acquire beneficial STMs might be difficult to observe.
Many more careful observations of EPCs and of birds outside of their breeding
seasons are required before our hypothesis can be properly evaluated.
The observations that extrapair mating systems are more common among
synchronously breeding songbirds than among asynchronously breeding songbirds
and more common in the temperate zone than in the tropics
(Stutchbury and Morton, 1995)
are consistent with our hypothesis. Synchronous breeding and the short
breeding seasons of the temperate zone limit the dispersal opportunities of
microbes and thus favor the evolution of less virulent strains of pathogens
(Ewald, 1994). We predict that
copulations, including EPCs, will be more common when the probability of
transmission of pathogenic microbes is low. In contrast, asynchronous breeding
and the long breeding seasons of the tropics provide more dispersal
opportunities for microbes and thus favor the evolution of more virulent
strains of pathogens (Ewald,
1994). We predict that copulations, including EPCs, will be
relatively uncommon when the probability of transmission of pathogenic
microbes is high.
We also predict the evolution of female traits that facilitate colonization
by beneficial microbes and impede colonization by pathogens obtained via
copulation. First, females in a variety of bird species have the ability to
selectively retain or expel ejaculates based on the identity of their
copulatory partner (Adkins-Regan,
1995; Birkhead and
Møller, 1992). Thus, we predict that females will be found
to be able to retain or expel semen based on whether it contains beneficial or
pathogenic microbes, respectively. Second, we predict the existence of
mechanical and physiological impediments to colonization by pathogenic STMs in
female reproductive tracts. For example, human females have a variety of
defenses that help them avoid being colonized by pathogenic STMs (reviewed in
Holmes et al., 1990;
Profet, 1993). It is highly
probable that females in all species with internal fertilization have evolved
defense mechanisms to prevent colonization by pathogenic STMs.
Here we provide a short list of some ways to test our hypothesis:
- Potential beneficial or pathogenic STMs can be identified by the
association between their presence and/or abundance on host health, growth,
social status, development of secondary sexual characters, and reproductive
success.
- The effects of experimental cloacal inoculation on individual health,
growth, status, and expression of secondary sexual characters and on
reproductive success could provide a direct way to identify both beneficial
and pathogenic STMs.
- Observations of the copulatory behavior of females of different ages could
be used to determine whether younger females copulate more frequently with
each partner and/or have more partners than older females on the grounds that
younger females need to be "vaccinated" against future infections
because of a lack of prior exposure to pathogens.
- An experiment that induces copulations outside of female fertile periods by
females that have been experimentally infected with pathogenic STMs could show
that females pursue copulations as a way of acquiring beneficial STMs.
ACKNOWLEDGEMENTS
We thank C. J. Bajema, two anonymous reviewers, and especially L. L. Wolf for comments on previous versions of the manuscript. M.P.L. benefited from conversations with P. W. Turke. M.P.L. was supported by a sabbatical leave from Grand Valley State University during the writing of the manuscript.
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