Download Adaptive resemblance: a unifying concept for

Biological Journal of the Linnean So&& ( I993), 48: 299-3 17.
Adaptive resemblance: a unifying concept for
mimicry and crypsis
ANDREW STARRETT
Department of Biology, Calzfornia State University, Northridge, Calzfornia 91330,
U.S.A.
Received 16 September 1991, accvpted for publication 10 Januacv 1992
Adaptive resemblance (AR) is a broad and inclusive concept which requires that only one condition
be met: that members of a species of organism gain fitness due to a selective advantage imparted by
a resemblance to some cue or signal in the organism’s environment. Essential to the evolution and
maintenance of AR is the dynamic and ongoing relationship among model, mimic and selective
agent (SA) that provides a complex selective milieu within which evolves resemblance. Because
specifics of a resemblance, including phenotypic traits being imitated, the nature of the model, and
the function of the resemblance, are not relevant to the concept of AR, the diversity and abundance
of such resemblances are limited only by the diversity and abundance of exploitable model-SA
relationships. Defined as it is by a single mimic-related criterion, AR thus provides the basis for
uniting under one conceptual umbrella diverse resemblances that range from rryptic to sematic,
interspecific to intraspecific, organismal to molecular, and material to attributive or implied. T h e
defining criterion excludes incidental resemblances which are contrastingly defined as those which
are the result of coincidental phenotypic responses to functional requirements or to other selective
influences. Some adaptive resemblances are attributable to more than one selective factor and thus
may be categorized in more than one way (having aposematic and procryptic functions, for
instance), while some others apparently are due to incidental resemblance as well as adaptive (such
as thermoadaptive and procryptic functions).
ADDITIONAL KEY WORDS:--Aposematism
Miillerian mimicry.
~
Batesian mimicry
~
deception
-
imitation
-
CONTENTS
. . .
Introduction . . . . . . . . . . . . . . . .
Adaptive resemblance .
. . . . . . . . . . . . . . . .
Applications of AR to troublesome categories .
. . . . . .
. . . . . . . . . . . .
Crypsis vs mimicry (sensu stricto) .
. . . . . .
Miillerian resemblance: mimicry or not? .
. . . . . . . .
Social mimicry and vocal mimicry
. . . .
Multiple roles of AR . . . . . . . . . . . .
Limits of AR .
. . . . . . . . . . . . . .
Molerular level of organization .
. . . . . . . .
Intraspecific resemblances
. . . . . . . . . . . . . .
Abstract models .
. . . . . . . . . . . .
Behavioural complexity .
. . . . . . . . . . . . . .
Discussion
. . . . . . . . . . . . . . .
Diversity and abundance of ARs is limited only by diversity and abundance of
. . . . . . .
exploitable model-SA relationships .
Increased evolutionary complexity is caused by three-party system .
Acknowledgements
. . . . . . . . . . . . . . . . .
References
. . . . . . . . . . . . . . .
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A. SI‘ARRE?‘?’
INTRODUCTION
Since 1963, a number of publications have provided overviews of the literature
dealing with the less-than-uniformly defined concept of mimicry. In particular,
those by Brower (1963, l988a), Wickler (1968), Rettenmeyer (1970),
Vane-Wright
(1976,
1980),
Matthews
(1977),
Wiens
(1978),
Cloudsley-Thompson, Edmunds, Endler, Robinson and Rothschild (all 1981, in
response to Vane-Wright, 1980), Pasteur ( 1982), Dafni ( 1984), Bowers ( 1988),
Stowe (1988), Gosliner & Behrens (1990) and Malcolm (1990) present a
reasonably representative picture of the current status of studies focusing on
mimicry and related concepts. Further, they make it apparent that ( 1 ) an
extremely wide range of relationships, systems and syndromes have been
included under the heading of ‘mimicry’, (2) there is a lack of unanimity
regarding some of the concepts involved in discussing mimicry, and (3) there is
no uniform theoretical base for an inclusive concept of mimicry (sensu lato).
For the most part, the best documentation and most of the experimentation
and development of theory have involved Batesian or Batesian-Mullerian
systems and cryptic resemblances (Brower, 1988a; Malcolm, 1990; Endler, 1984,
1988, 1990). Establishing that a given resemblance represents mimicry, by
whatever definition, is difficult, and even more so when it involves something
other than a Batesian or Mullerian relationship. For this reason, much of the
descriptive literature is anecdotal and speculative, involving explanations that
are often intuitive. However, the great variety of mimicry systems (Pasteur,
1982), and such thought-provoking papers as those by Matthews (1977),
Rothschild ( 1979, 1981, 1984), Barnard ( 1984), Lloyd ( 1984), Janzen ( 1988b)
and Malcolm (1990), help to stimulate thinking about where the limits to the
concept of mimicry ought to be. Therefore, in an attempt to provide an inclusive
conceptual framework for the vast array of phenomena that can come under the
rubric of mimicry, I am offering the concept of ‘adaptive resemblance’. It is a
potential answer to the need expressed by Rothschild (1981): ‘The ever
expanding field of mimicry requires a clear, but very elastic, definition which
avoids hair splitting but allows for the constant stream of examples and concepts
which may be fitted into a series of special categories--many of which merge
into each other’. The definition of this concept brings together the vast numbers
of cases, known and as yet undescribed, of mimicry and crypsis (as generally
understood) into one great array of related phenomena which may well
constitute the largest single class of adaptations, at least within vertebrates,
arthropods and opisthobranch gastropods, and one that is certainly among the
most important, especially in tropical environments (see Gilbert, 1983; DeVries,
1987: 20-22; Gosliner & Behrens, 1990).
It is my intent in the exposition that follows to define and characterize
adaptive resemblance, to demonstrate the capacity of this concept to encompass
a broad spectrum of resemblances and to discuss the implications that derive
from the definition. T h e presentation of a minimal and basic paradigm to
illustrate one way in which various types of resemblance can be included under
one umbrella should not be interpreted as a criticism of other classifications;
rather, it should be seen as a vehicle for emphasizing the interrelationships
among such resemblances. The use by different authors of a variety of equally
valid and justifiable diagnostic criteria for categorizing and ordering mimetic
ADAPTIVE RESEMBLANCE
30 I
and cryptic resemblances can only enhance appreciation and understanding of
the spectrum of phenomena that can be included under the definition of
adaptive resemblance (cf. in particular, Vane-Wright, 1976; Endler, 1981;
Pasteur, 1982).
Frequent documentation by reference to the excellent review by Pasteur
(1982) rather than to each primary source separately, was done in the service of
bibliographic economy. For the same reason I omitted references to works of
many of the important early founders and developers of the field of mimicry in
the broadest sense. The names of these seminal contributors to the observational,
experimental and theoretical bases of current activity in this area, G. D. H.
Carpenter, C. A. Clarke, H. B. Cott, E. B. Ford, Karl Jordan, Guy Marshall,
E. B. Poulton, P. M. Sheppard and C. F. M. Swynnerton, to pick out some of
the most noteworthy, are to be found throughout the literature citations in the
papers to which I have referred (especially Cott, 1940; Brower, 1963), if not cited
below.
ADAPTIVE RESEMBLANCE
Adaptive resemblance (AR) is defined as: any resemblance that has evolved,
or is maintained, as a result of selection f o r the resemblance. A particular colour
pattern or other phenotypic characteristic that resembles that of another
organism or an inanimate object, for instance, and results in increased fitness for
the resembler as a consequence of the resemblance, qualifies as AR. It is the
effectiveness of the resemblance which determines the selective advantage
bestowed by the adaptation. The concept includes all cases of resemblance that
meet the single condition imposed by the definition.
The definition of AR could, and perhaps should, be extended to include the
tripartite system of elements that are essential to the evolution and maintenance
of all of the phenomena that qualify under the definition. Among these more-orless interactive elements, the ‘signal receiver’ or ‘R’ (Wickler, 1965), ‘dupe’
(Pasteur, 1972) or ‘operator’ (Vane-Wright, 1976), is the selective agent (SA) that
drives the system; the model (‘S,’,Wickler, 1965) may be any characteristic signal
or signature that is compatible with the sensory and neurological, or
immunological, capabilities of the SA provided by just about any component of
the mutual environment (internal or external) of both mimic and SA; and the
mimic (resembler) (‘S2’,Wickler, 1965) may be any species of organism or virus
capable of producing the appropriate mimetic signal or signature (see also
‘detector’, ‘detectee’ and ‘background’ of Barnard, 1984). The SA is necessarily
a species of animal, or a group of species of animals having a common
relationship with the mimic (i.e. as predators or possible prey); the mimic must
be a living organism or virus (or group, part or product thereof); and the model
may be living or dead (an organism, or group, part or product thereof), animate
or inanimate, organic or inorganic, specific or generalized, even indirect, implied
or attributive (Hespenheide, 1973; Pasteur, 1982; Lloyd, 1984; Rothschild, 1984;
Caldwell, 1986; and specific examples below under ‘Limits of AR’--‘Abstract
models’). In the ‘purest’ cases of AR, the resemblance depends upon the model,
which supplies the basic pattern to be copied, and the sensory and behavioural
characteristics of the SA(s), which determine the degree of preciseness required
in order for the resemblance to be effective.
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A. S‘TARRETr
It should be obvious from the previous paragraph that neither the nature of
the model nor the function of the resemblance are relevant to the definition of
AR, although they do have relevance to further consideration of the various
phenomena that are brought together within this inclusive concept. I t is also
important to understand the distinction between a resemblance and the
phenotypic characteristics that comprise it since neither are the specifics of the
resemblance of relevance to the concept of AR. An ‘honest’ aposematic colour
pattern (i.e. one backed up by a memorable defence) only qualifies as an AR
(i.e. Miillerian mimicry) when it resembles that of another organism, although
such a suite of characteristics would be functional whether or not a resemblance
existed.
The definition of AR excludes incidental resemblance or convergence ( I R )
which is due to common adaptive responses to functional requirements, (green leaf colour
in plants, conical bill shape in seed-eating birds or thermoadaptive colouration
in animals, to cite a few examples) or to other selective processes (Hamilton,
1973; Rothschild, 1975, 1981; Endler, 1978, 1981; Berger & Kaster, 1979; Burtt
& Gatz, 1982; Orians, 1985). This is not to say, of course, that there may not be
more than one function or adaptive value to a particular phenotype. Adaptive
and incidental resemblances can, and do, coincide (Endler, 1981; Rothschild,
1975, 1981; and more under ‘Multiple roles of AR’ below).
APPLICATIONS OF AR TO TROUBLESOME CATEGORIES
The general concept of adaptive resemblance is not really novel, dating at
least from Bates (1862) (see Pasteur, 1982: 171, 173), and the intent of my
definition is already implicitly involved in the interpretations of many of the
described cases of mimicry, in its broadest usage. The specific character of this
definition allows the inclusion of a broad spectrum of relationships that need
have only one thing in common: the adaptive value of a resemblance. The
following discussions of some of the controversial, marginal or otherwise
troublesome conceptual areas should help to illustrate the unifying nature of this
inclusive definition of mimicry (sensu lato). Hereafter, specific examples,
references or quotations which are documented by ‘Pasteur’ without the year or
by pagination only, refer to Pasteur (1982).
Crypsis us mimicry (sensu stricto)
Adaptive resemblance is really a two-word definition of mimicry (sensu lato);
my definition of AR explains the significance of the unifying concept involved.
However, I chose to use adaptive resemblance, rather than the term mimicry, to
represent a ‘new’ inclusive concept, because the latter has accumulated so many
definitions that its use might interfere with the acceptance of the umbrella
concept. One such conceptual barrier to using mimicry as a n inclusive term is
the common practice of separating cryptic resemblances, such as camouflage,
background matching, disruptive patterns and other types of resemblance that
involve non-living or inanimate models, from ‘true’ mimicry, as typified by
Batesian resemblances (Pasteur, 1982: discussion, fig. 1). However, most
resemblances falling within the broadest definitions of crypsis fit my definition of
AR and should be accepted as part of the unified concept (in agreement with
ADAPTIVE RESEMBLANCE
303
Bates, 1862; Wiens, 1978; Pasteur, 1982; among others). I t is, in these cases, as in
those involving non-cryptic resemblances, the resemblance that bestows the adaptive
advantage on the mimics, not the nature of the model.
Along with the wide range of interpretations of the concept of mimicry goes a
similar lack of agreement as to what constitutes crypsis, one result being that
there is no consensus as to the criteria for dividing cryptic from non-cryptic
resemblances (summarized by Endler, 1981; Pasteur, 1982). However, there does
seem to be one logical and consistent basis for distinguishing between these two
basic types of AR and that is the behaviour of the SA towards the mimic
(Endler, 1981; Barnard, 1984; see also Edmunds, 1981; Zabka & Tembrock,
1986). If the resemblance functions so that the mimic elicits no response from the
SA, either because the mimic is not noticed or because it is ignored (not
recognized) by the SA even if perceived, then the resemblance is cybtir ( =
hidden; effectively, ‘hidden in plain sight’); if the resemblance operates so as to
elicit from the SA a predictable response that is advantageous to the mimic, then
the resemblance may be said to be sematic ( = signalling; the equivalent of
mimicry in the more common, less inclusive sense). This distinction, which is
essentially conceptually that used by Poulton (1898) and Pasteur (pp. 181-182),
avoids problems with the nature of the model, which may still be addressed by
using subordinate categories. For example, my own preference is to base the next
rank of categories on a combination of proximate (the SAs response to the
mimic) and ultimate (trophic [ = predatory = aggressive], defensive [ =
protective], or reproductive) functions of ARs. T h e resulting paradigm (terms
adapted from Poulton, 1890) provides a consistent conceptual classificatory
framework for all cases of AR, with the use of further subcategories or
subdivisions to suit personal preferences. Thus:
Adaptive resemblance-defined above.
Cryptic resemblance-mimic not noticed, or ignored; does not appear to be
what it is.
Procryptic resemblance-defensive function.
Anticryptic resemblance-trophic function.
Sematic resemblance-mimic
elicits predictable, advantageous response
from SA; appears to be what it is not; based on established signals of
models.
Aposematic resemblance-defensive
function; warning, promotes
avoidance of mimic by SA.
Episematic resemblance-trophic,
defensive, reproductive functions;
alluring or pacifying, promotes acceptance and allows or encourages
approach by mimic or SA.
Poulton ( 1890) used pseudaposematic and pseudepisematic to distinguish
‘false’ warning and alluring colourations from those that do not represent ARs. I
prefer to repeat ‘resemblance’ after aposematic and episematic, as I did for the
other categories in the paradigm, as a means of emphasizing the relatedness
among the components and the umbrella concept and because not all episematic
and aposematic signals in mimetic systems are false. Of course, AR is not limited
to resemblances involving colour patterns.
The three ultimate functions employed in the preceding schema represent the
three major life functions into which all others may be subsumed. Their use is
arbitrary and does not imply that there are not other equally useful and
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A. STARKETT
appropriate ways of categorizing basic functions; Wiens uses four (1978),
Pasteur, seven (p. 176), for example.
Mullerian resemblance: mimicry or not?
The exclusion of Mullerian resemblance from consideration as a type of
mimicry has been actively promoted on several grounds (see Wiens, 1978;
Pasteur, 1982; for summarizing discussions of the controversy). The most
commonly repeated objection to including resemblance between protected
species as a form of mimicry is that no deceit is involved (Wickler, 1968; Pasteur,
1982; ‘failure to discriminate’-Wiens,
1978), so that predators (SA) can only
benefit from the mimics’ use of a common warning signal that reduces energy
expenditure and negative experiences required to sample potential prey species.
It seems clear to me that the function of mimicry (AR) is to provide an adaptive
advantage to the mimic; that the SA benefits in this type of relationship is
irrelevant. For Mullerian or Batesian mimicry to be effective, a predator (SA)
must respond to what it perceives to be one and the same warning signal that it
has learned to avoid by previous experience (aspect discrimination vs species
discrimination, Matthews, 1977), or that calls forth an innate response
(Guilford, 1990). The response should be the same (avoidance) whether the
predator encounters a protected species (the model or a Mullerian mimic) or an
unprotected one (a Batesian mimic), and the relevant taxonomy in regard to the
potential prey fauna at any given time may include as few as two ‘species’
(aspects): one to be eaten, the second to be rejected (see also Janzen, 1988a, b;
Chai, 1990). Deception (deceit, failure to discriminate, presumably as a result of
successful deception) is obviously involved in the success of the Batesian mimics,
which are included in the second ‘species’; should that ‘species’ represent a
synaposematic complex [i.e. a group of species or individuals, whether protected or
not, which utilize a common set of warning signals (Huxley 1934, applied to
Mullerian mimicry), including both Mullerian and Batesian mimics], only an
entomologist would be able to discriminate among all species involved, and even
then would not necessarily know which were protected and which were not
without prior knowledge or further information (see also Guilford, 1988).
Furthermore, the selective advantage gained by member species in a Mullerian
system is presumably due to the inability of a predator to discriminate (but see
Huheey, 1988), thereby reducing the per species exposure to sampling attacks.
Thus, to answer Wiens’ ( 1978) further concern, based on ‘lack of distinction
between model and mimic’, there probably would be no single species model in
the system. For any individual predator, one could say (as did Turner, in
different terms, 1977) that the species which first provides a sufficiently negative
experience to initiate a n aspect avoidance response becomes the model in that
case. However, reinforcement through further sampling could involve other
‘model’ species in the system. The initial, and possibly further, contacts would
depend upon escape behaviours, strength of protection and relative abundances
of the Mullerian species in the predator’s environment (discussion in Matthews,
1977). Of course, each predator responds uniquely to each member of a
synaposematic complex: forgetful and particularly hungry predators,
discriminating predators and those with differing tastes or tolerances for the
chemical defences in their various dosages among prey species (Brower, Alcock
ADAPTIVE RESEMBLANCE
305
& Brower, 1971; Rothschild, 1979; Malcolm, 1990) serve to make such systems
dynamic.
Points raised in discussions concerning the differing effects of various selective
forces in the evolution of Batesian vs Mullerian mimicries (Huheey, 1976, 1980,
1988; Benson, 1977; Sheppard & Turner, 1977; Rothschild, 1979; Malcolm,
1990), while providing information about the relationships included under
Miillerian mimicry, do not argue against an adaptive value to Miillerian
resemblance. It seems clear to me that the resemblance among Miillerian mimics
evolves, or is maintained at least, through the proximate selective advantage of
the resemblance (Turner, 1977), thus fulfilling the definition of AR. Mullerian
mimicry falls within the category aposematic AR, along with Batesian mimicry
and many of the ‘virtual’ (Pasteur, 1982) resemblances that have been (may be)
included under AR.
In much of the preceding discussion the term ‘arithmetic’ could be substituted
for Mullerian, since the two concepts, Miillerian and arithmetic mimicry (van
Someren &Jackson, 1959), are similar enough to call forth the same objections
to their being included under mimicry (Wiens, 1978; ‘non-deceitful homotypies’
of Pasteur, p. 193). However, while not aposematic in the same sense as
Miillerian mimics, the collective presence of arithmetic mimics may, through
reinforcement by frustrating experiences of predators, take on a negative or
warning significance, i.e. a ‘reputation’ for providing poor returns for energy
expended in attempting captures. A reasonable complementary explanation is
provided by Endler’s (1988) contention that individuals of schooling and
aggregating non-aposematic species may be cryptic against a background of
conspecifics. T o echo Pasteur (p. 194), more investigation of this phenomenon is
needed.
Another source of resistance to accepting Miillerian resemblance as a form of
mimicry may stem from confusion of Mullerian mimicry with aposematism.
While the latter is requisite for the former, warning signals associated with
protective adaptations have evolved in diverse groups of organisms, by several
evolutionary routes, without serving as models for mimetic systems. However, in
some cases groups of species (i.e. Mullerian mimics) have gained selective
advantage through sharing the same or similar warning signals in an ongoing
dynamic relationship with specific predators. Such mimicry of aposematic signals
is certainly AR, but aposematism exists as a distinct phenomenon whether
mimicry is present or not (see also Rothschild, 1979; Malcolm, 1990).
Social mimicry and vocal mimicry
The concepts of social mimicry (Moynihan, 1968) and vocal mimicry (Baylis,
1982; not acoustic eucrypsis or non-vocal homophony, pp. 184, 189) have both
encountered some difficulty with delimitation and content, as well as acceptance.
Pasteur (p. 173) rejected social mimicry as ‘mere convergence’ having ‘no signal
receiver, not to mention dupe’ (both = SA), but then applied the term in two
different contexts (pp. 179, 186-187); vocal mimicry he also rejected, apparently
because he interpreted it as being ‘conscious imitation’, which places it outside of
his quite inclusive, self-defining terminology ‘unconscious biological mimicry’
(p. 168) (almost = AR). My view of these two categories is that most of the
described mimetic systems that have been proposed as either social or vocal
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A. S’T.4RRETl
mimicry (and there is overlap) qualify under the definition of AR; the problems
come from differences in interpretation of the significances of the mimicries
involved and lack of agreement as to what should be included in each category
(social-Moynihan, 1960, 1962, 1968, 1981; Barnard, 1979, 1982; Ehrlich &
Ehrlich, 1973; vocal--Baylis, 1982; Hartshorne, 1956; Nicolai, 1974; Robinson,
1974; Krebs, 1977; Payne, 1983). Addressing these problems requires
identification and rejection of coincidental convergences as well as determination
of the ultimate functions of the various resemblances described.
In the case of social mimicry, the number of examples attributed to this type of
resemblance is limited, but there exists a variety of described systems and
convergences that may, in fact, be included within the concept (Wickler, 1968;
Pasteur, 1982; as well as references just cited). Vocal mimicry, on the other
hand, has an extensive literature that provides a large number of examples as
well as a number of explanations for its significance, as exemplified by (but not
limited to) the citations in the previous paragraph. Vocal mimicry, which is here
understood to exclude other forms of acoustic mimicry, is essentially limited to
birds and mammals, possibly due to structural-functional constraints. Unique to
vocal mimicry is the ‘conscious imitation’ vs ‘unconscious mimicry’ issue
(Pasteur, p. 173; also Andrew, 1962) and the related fact that, at least in the
cases of most mimetic vocalizations in birds, porpoise ‘vocal’ imitation and
human vocal ‘mimicry’, the ability to imitate and the propensity to do so are
inherited and not the specific signals imitated.
Multiple roles of AR
The recognition that there may be more than one possible interpretation of
phenotypic features that have been diagnosed as cryptic or sematic adaptations
can raise doubts concerning the validity of the initial interpretation: perhaps the
characters really represent I R instead of AR. However, as pointed out by
Rothschild (1975, 1981) and Endler (1981), AR and I R can coincide in the
same organism, representing a combined response to more than one selective
influence. The limited selection of illustrative examples that follows, when added
to those presented by Rothschild (1975, 1981, 1984) and Endler (1981),will help
to demonstrate the spectrum of possible interpretations that may be valid for
different types of ARs.
The first of these examples belong to the group of cryptic organisms that
resemble definable models (mimesis, Pasteur, p. 183). The distinction between a
component of an organism’s environment that is ignored because it is not
recognized as being what it is ( a cryptic edible caterpillar, for instance) and one
that is passed by because it is ‘recognized’ as being something it is not ( a sematic
twig or bird-dropping mimic) and therefore not energetically worth sampling, is
impossible to discriminate objectively in most cases. However, the difficulties
encountered with the distinction just exemplified, between procrypsis involving
definable models and one type of aposematic resemblance, stem from lack of
knowledge as to the learning characteristics and foraging behaviours of potential
predators (SAs) rather than from the definitions of cryptic and sematic AR.
That the distinction can be tenuous in some cases, the same AR conceivably
even belonging in both categories simultaneously depending on circumstance,
only makes adaptive resemblance, which readily accommodates this intriguing
ADAPTIVE RESEMBLANCE
307
apparent impasse, more challenging: learn more about predator characteristics
that allow the efficacy of twig mimicry, bird-dropping mimicry and other types
of AR that seem to be situationally cryptic or sematic! An insectivorous bird that
is a neophobic specialist might never challenge a bird-dropping and, thus, would
never discover a whole class of procryptic edible insects, whereas a more
adventuresome or meticulous generalist might occasionally sample birddroppings and thereby reinforce an avoidance image, thus providing protection
for a whole (the same) class of aposematically signalling edible insects. The
predators just evoked are non-fictional (Greenberg, 1983) and, although the
scenarios involving them may rarely occur (Robinson, 1981), the possibility does
exist that a particular resemblance may provide both cryptic and sematic
protection against a spectrum of potential predators.
The foregoing discussion provides an illustration of a case in which a single
adaptation may represent a compromise among responses to more than one
selective influence, e.g. in the case of bird-dropping mimicry, two different types
of predatory behaviour that usually select for different defensive adaptations. A
more complex version of bird-dropping mimicry is provided by tropical
Australasian thomasid crab spiders (Phrynarachne decipiens Forbes) that add smell
to the visual image, thereby possibly enhancing the aposematic message and
adding an aggressive episematic function by attracting coprophilous insect prey
(Gray, 1990).
Resemblances showing even greater complexity may be illustrated by two
additional selected examples. Based on illustrations in Wickler (1968), Owen
(1980) and Ross & Kuhn (1984), it seems probable that flower-mimicking
mantids (Orthoptera: Mantidae) may represent as many as three types of AR, in
various combinations of procryptic-an ticryptic-aggressive episematic, in their
resemblances to flowers (Hymenopus coronatus [Olivier] , Pseudocreobotra wahlbergi
Stal) or ‘flowerness’, with the nymphal stages possibly differing from the
imaginal stages in these functions. According to Springer & Smith-Vaniz (1972),
each of three interacting species of Red Sea blennies (Osteichthyes: Blenniidae)
may play one or more mimetic roles (Batesian, Miillerian or aggressive
episematic) depending upon which of the other two species is involved; one of
the species is said to represent all three types of mimicry mentioned!
The last two complexes, each of which includes mixed species flocks of moreor-less similarly coloured non-breeding birds, represent combinations of AR and
IR. A number of species of shorebirds (Scolopacidae and Charadriidae), which
regularly flock in various species combinations during the non-breeding season,
have remarkably similarly coloured plumages that also appear procryptic
against the substrates on which they feed and roost. T h e interspecific
resemblance may function as social episematic AR, facilitating interspecific flock
cohesiveness and other mutually benefiting social interactions (Moynihan, 1968,
or Barnard, 1984) while at the same time it represents syncryptic (coincidental
procryptic) responses to potential predation (procryptic AR) in each of the
species. The ultimate significance of arithmetic mimicry may also be found in
these flocks in many species of which even sex and age differences are minimal
(requiring careful scrutiny by experienced human observers) (but see Endler,
1988: 509). In the case of the dark coloured species of North American
blackbirds (Emberizidae: Icterinae), on the other hand, sex and age differences
in plumage colouration do exist, though all plumages tend to be dark hued and
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A. S’I‘ARRWT
minimally distinguishable from a distance. The various species apparently bring
highly developed monospecific flocking behaviour to the mixed species flocks
which may be considered also to provide examples of social episematic AR.
Further, Orians (1985) suggests that there may also be coincidental procryptic
function (my terminology) to the dark colouration, when the birds are roosting
or on nests, as well as coincidental thermoadaptive function (also Hamilton,
1973).
LIMITS OF AR
Limits of acceptability of proposed and potential resemblances are seen in four
areas in which specific aspects of the resemblances make unequivocal diagnoses
difficult. A brief discussion of these areas will help to identify the questions raised
by each.
Molecular level of organization
While molecular mimicry (sensu Damian, 1964; see also Bloom, 1979; Moore et
al., 1990; Goodenough, 1991) has been generally accepted as a subset of
organismal mimicry (p. 178), the diagnosis becomes less clear in cases in which
plants produce compounds that can mimic the effects of insect (Williams, 1970;
Bowers, 1980) or mammalian (Shutt, 1976) hormones, possibly as a defence
against herbivory, or those in which butterflies make other possibly mimetic
compounds (e.g. ‘chemomimicry’ of Brown, 1967; see also Stowe, 1988;
appendix B ) .
IntraspeciJic resemblances
Intraindividual IAR ( = ‘self-mimesis’, p. 178), which involves different parts
of the same individual, comprises a disparate assortment of phenomena that
include behavioural (Aristotelian mimicry, p. 184; thanatosis, p. 190) and
colour-based (Wicklerian-Guthrian mimicry, pp. 167-1 68) resemblances, to
which should be added the various ARs which come under the general heading
of ‘head-and-tail’ mimicry and are found in some species of snakes (p. 192),
butterflies (Wickler, 1986) and, possibly, fish having a single ‘eyespot’ at the base
of the tail. Interindividual IAR ( = ‘automimicry’ of Pasteur, p. 178), on the
other hand, includes resemblances among individuals of the same species, which
fall readily into three subgroups according to the relationships between mimic
and model. Intrasexual mimicry (1) may be found among individuals of the
sexually selected sex in many dimorphic species of animals, as suggested by
Rohwer, Fretwell & Niles (1980) for male red-winged blackbirds (Agelaius
phoeniceus [Linnaeus]); there may well be selection for resemblance to the
phenotypic characteristics that represent to the selecting sex the most successful
individuals in terms of potential inclusive fitness (but see ten Cate & Bateson,
1988). In intersexual mimicry (2), one sex mimics characteristics (or eggs) of the
other (Wicklerian, Bakerian and Wicklerian-Barlowian mimicries, pp. 186, 190191; Thompson, 1991; examples cited in Halliday & Slater, 1983: 69, 170-1 7 1,
173-1 75).
A third type of interindividual IAR, which appropriately might be called
ADAPTIVE RESEMBLANCE
309
‘conspecific mimicry’ (3), involves resemblances among individuals in a
population, irrespective of sex, and even age in some species. A high degree of
uniformity, in colour pattern for example, in a population suggests that rather
finely tuned stabilizing selection is operating that results in resemblance among
individuals. In many, if not most, cases of cryptic AR, close resemblance among
cryptic conspecifics is due to AR indirectly as an incidental consequence of
selection for limited variability among cryptic individuals and is not in itself AR.
O n the other hand, uniformity among individuals of an aposematically
patterned species could well be due to selection for resemblance to the most
effective warning pattern, i.e. that which is most easily remembered or is
associated with the most effective deterrent. Individuals of any protected
aposematically signalling species, then, could be considered to be Mullerian
mimics of one another. One could further probe the limits of AR by suggesting
that, in terms of the taxonomy of a particular predator, all protected individuals
among the species in a synaposematic complex ( = a single aspect or ‘species’)
would also be Mullerian mimics of one another. This interpretation would make
the well-known monarch-queen-viceroy butterfly relationship a complex and
dynamic synaposematic system with the roles of model and mimic varying under
the combined influences of a toxicity-palatability gradient involving different
populations, and even individuals, of the monarch (Danausplexippus [Linnaeus]),
as well as the queen ( D . gilippus [Cramer]) and viceroy (Limenitis archippus
[Cramer]), and toxicity tolerances or ‘taste preferences’, feeding techniques and
hunger states of the various predators (SAs) which attack the butterflies in the
complex (Rothschild, 1979; Bowers, 1988; Brower, 1988b, 1992; Whitman, 1988;
Malcolm, 1990; Ritland & Brower, 1991; but see Lloyd, 1984: 50).
Although originally applied to intraspecific Batesian mimicry in monarch
butterflies (Brower, 1969) and used principally in that context since (e.g.
Lincoln, Boxshall & Clark, 1982), the term ‘automimicry’ has also been
generalized to label various types of intraspecific mimicry, both intraindividual
(e.g. Gans, 1987; Guthrie & Petocz, 1970) and interindividual (e.g. Stiles, 1979;
Sordahl, 1988; Pasteur, already cited in this section). In addition, there seems to
be some question as to whether any monarchs are completely without chemical
protection (Rothschild, personal communication; Ackery & Vane-Wright, 1984:
92; see also Gibson, 1989). I agree with Rothschild (1979: 93) in advocating use
of Pasteur’s (1972) designation ‘Browerian mimicry’ in preference to
automimicry for the mimetic relationships among the variably protected
individuals of monarch butterflies.
Abstract models
Two separate gradients, based on degree of abstractness of models, are
discussed here: the first involves cryptic resemblances, the second, sematic.
In Pasteur’s classification of cryptic resemblances, ‘mimesis’ requires models
that are defined, identifiable elements of the environment (p. 183), and
‘eucrypsis’, undefined characteristics of the general background (p. 182). A
number of devices have evolved to make the eucryptic mimic unrecognizable
against a particular background, among which are included colour and pattern
matching, outline modification or obliteration, shadow reduction, obliterative
shading and disruptive colouration (Cott, 1940). Many of these dissembling
310
A. SI‘ARRE1“T‘
adaptations, which emphasize the ‘not appearing to be what one is’ aspect of
crypsis (i.e. what could be called ‘adaptive dissemblance’), disguise the physical
characteristics of organisms and help them match their backgrounds. The critical
question arises at this part of the crypsis abstractness gradient: is it possible for a
dissembling pattern, for instance, simply to interfere with a predator’s ability to
recognize a potential prey item because it does not fulfil a specific search image
(Lloyd, 1984: 60)? Can there be adaptive dissemblance without AR? Endler
(1981) contends that, in the case of an organism that would be cryptic without
disruptive markings, adding them merely substitutes one cryptic pattern for
another.
Pasteur (pp. 191- 192), in an attempt to reduce the hodge-podge of possible
sematic resemblances having more or less abstract models to a conceptually
ordered system, included most of these in the category ‘virtual model’ [model not
an actual species, but may be defined (‘semi-abstract homotypy’) or not
(‘abstract homotypy’)]. The proposed resemblances included by Pasteur, plus
numerous others, can be arranged in such a way as to present an abstractness
series that corresponds with decreasing likelihood of qualifying as AR, by
grouping them under three headings. Distinctive resemblances, readily accepted as
AR, suggest or recall characteristics of some generic, or even specific, model; this
category includes most of the semi-abstract virtual homotypies of Pasteur, cited
above. Altributive resemblances, reasonably interpreted as AR, are a bit more
abstract than the preceding, suggesting or recalling attributes associated with
some innately recognized or previously experienced signal; included are some
representations of eyes, placed so as to evoke (possibly) the image of a predator;
examples of ‘aide mkmoire’ mimicry of Rothschild (1984), injured prey [broken
wing displays by nesting birds (‘intraspecific Aristotelian mimicry’ of Pasteur,
p. 190)], dead prey [‘self-mimesis ( = thanatosis)’, p. 1841, fighting reputation
(Caldwell, 1986), reputation for ability to escape (from SAs) (Hespenheide,
1973), and chemical and thermal lures used by plants to attract pollinators
(Dafni, 1984). Imblied resemblances, questionably interpreted or marginally
acceptable as AR, including a variety of novel, startling and/or distracting
displays and signals which are mainly effective when used against neophobic or
xenophobic predators, such as many species of birds (references in Matthews,
1977: 2 14); included are suggestive eyespots, often placed in inappropriate places
and/or inappropriate numbers (e.g. on peacock fans); interspecific threat
displays; protean displays (Humphries & Driver, 1970); and Matthews’ (1977:
214) apostates that ‘are mimics-not of models’ signals, but of the fact that
models signal’.
Deimatic displays (Edmunds, 1974), which Vane-Wright (1976) does not
accept as mimicries and Cloudsley-Thompson (1981) objects to as being invalid
associations of unrelated phenomena, are here found in both the first and the last
categories, and imitation eyes are found in all three.
Behavioural complexit3,
Behaviour, which tends to become increasingly complex in the
phylogenetically more advanced groups of organisms, is an integral part of the
majority of ARs involving animal mimics. The significant question in the present
context is whether there is, somewhere along the behavioural complexity
ADAPTIVE RESEMBLANCE
31 1
gradient, a point beyond which release from unconscious stereotyped behaviour
allows discretionary situational and consciously deceptive imitation that might
not be subject to natural selection. One point in the behavioural complexity
gradient where a significant change takes place is that at which imitative
learning becomes important. For birds and mammals, the ability to imitate can
be highly adaptive and, thus, subject to natural selection; in many species one or
more of the behaviours required for successful mating, rearing of young, foraging
or communication (song and vocal language) depend on imitation of parental
behaviour by their offspring (Bonner, 1980: 121; Konishi et al., 1989). Vocal
mimicry and other types of adult imitation perhaps represent ontogenetic
extensions of basic behavioural capacities that are frequently diminished or lost
after sensitive periods in many species.
With the previous discussion in mind, then, consider the following examples of
‘mimicry’ that might (or might not) be included within the concept of AR: the
imitation, by some species of parrots, of sounds of human speech and
vocalizations of other animals, as well as mechanical sounds produced by nonliving sources (extraspecific models unknown in the wild, Thorpe, 1972;
Foreshaw, 1977; Sparks & Soper, 1990); learning and use of a second language
by adult humans; the use of visual camouflage by soldiers, using the same
techniques employed in different engagements over several generations of
people; the striking ‘intraproduct’ similarity in appearance (packaging) of most
brands of certain products, such as peanut butter and breakfast cereals; hand
copying of ancient manuscripts by monks; and plagiarism. It is not the definition
of AR that causes the problems encountered in diagnosing the resemblances that
may be included within this concept in the cases mentioned in this section.
Rather, it is a matter of deciding which examples meet the criterion of
demonstrating a selective advantage for the resemblance in question. I favour
the interpretation that behavioural complexity is a consequence of the evolution
of animal nervous systems, and that behaviour is, in the final analysis, adaptive
(Bonner, 1980; Cavalli-Svorza & Feldman, 1981). If this is so, then ‘conscious
biological mimicry’ would have a place under the umbrella of AR, and examples
could be found of conscious aposematic, episematic, procryptic and anticryptic
imitations or deceptions (p. 173). Wickler (1968) included human examples in
his discussions, Vane-Wright ( 1976) did so in his classification.
DISCUSSION
The inclusive nature of the definition of AR and the essential involvement of
the ‘triumvirate’ (model, mimic = resembler and SA = SAs) in the origin and
destiny of any resemblance that qualifies as such suggest two corollaries that lead
to generalizations which can be made about this unique group of adaptations.
These corollaries are ( 1 ) that the range of diversity and the number of ARs is
limited only by the range of diversity and number of exploitable model-SA
relationships and (2) that the presence of a requisite third party in the selective
milieu adds a degree of complexity which in turn has implications for
evolutionary consequences to all three members of the triumvirate. While the
implications of these two corollaries are not entirely separable, they are more
conveniently discussed separately.
312
A. S’TARRETT
Diversity and abundance of ARs is limited only b~ diversity and abundance of exploitable
model-SA relationshibs
The term ‘exploitable’ implies mimetic capability on the part of the mimic as
well as appropriateness of the model-SA relationship and its susceptibility to
being utilized by a resembler; model-SA relationship includes indifference-no
response ‘behaviours’ by SAs toward cryptic models. Given these obvious
qualifiers, it is possible to examine a related generalization about AR which is
suggested by this corollary. There tends to be a reciprocal relation between
diversity and uniqueness that seems to apply to ARs: the diversity is in great part
a result of the uniqueness of the interactions among mimic, model and SA that,
to a greater or lesser extent, characterize each individual case (Rothschild, 1979;
Huheey, 1988). This diversity-uniqueness connection is attested to by the
diversity of evolutionary mechanisms and processes that are called upon to
explain specific cases and categories of AR. A sampling of this last type of
diversity may be found in Brower & Brower (1972), Turner (1976),
Vane-Wright ( 1976), Rothschild ( 1979), Gilbert ( 1983), Endler ( 1988), Guilford
(1988) and Malcolm (1990) to cite just a few.
Increased evolutionary complexity is caused by three-party system
From the resembler’s point of view, the model is the third party added to what
otherwise would be a ‘premimid-SA relationship involving the same SA or,
perhaps, a ‘generic’ group of SAs providing the same selective pressures as would
those forming the third corner of the AR system. If one assumes that an incipiect
mimic goes through a period of intense selective pressure during the transition
from one adaptive strategy to another (i.e. from one relationship with the SA to
another), being between peaks of effectiveness, then one can assume also that a
model which has a dynamic relationship with its SA, as is the case with sematic .
resemblances, will have a tendency to change in some way in response to
perturbations in this relationship such as might be caused by adding the evolving
mimic to it. This potential for the model to be under pressure to change in order
to gain relief from the added selective influence of the mimic, as may occur as a
consequence of Batesian mimics, may result in convergence becoming
advergence, which, then, requires the mimic to ‘chase’ the model (Brower &
Brower, 1972; Huheey, 1988; but see also Vane-Wright, 1976). The mimic
would thus be subject to a higher level of selective ‘harassment’ than if it were
dealing only with the SA, even when an effective degree of resemblance had
been attained by the mimic; while converging on the model’s aspect and then
maintaining an effective resemblance, the mimic could be said to be attempting
to hit a moving target while being more or less constantly jostled by the SA. At
this point it is obvious that the mimic is also adding pressures to the model’s
relationship with the SA and the SA is under increased pressure due to changes
in its relationships with both model and mimic. T h e influence of the model on
system dynamics differs in most types of cryptic resemblance in that it is not an
interactive member of the triumvirate. However, the presence of the mimic can
alter the SAs behaviour toward the model, and backgrounds and other types of
models can undergo alteration or fluctuations in availability due to seasonal
change, naturally occurring or human mediated habitat modification, or
ADAPTIVE RESEMBLANCE
313
fluctuations in populations of organisms that provide model cues for cryptic
species. Mimicry systems in which two or three members of the triumvirate
represent a single species (respectively, bipolar and conjunct systems: pp. 176,
182; Vane-Wright, 1976) presumably add another dynamic to the scenario due
to a potentially stronger selective imperative, the consequences of an imperfect
resemblance most likely being drastic. The dynamics of selective processes which
are responsible for the evolution of ARs, then, can be expected to differ, at least
quantitatively, from those producing other kinds of resemblance (IRs), and,
perhaps, other kinds of adaptations as well.
The mimic’s susceptibility to changes, in the model or its relation with the SA,
that reduce the effectiveness of the resemblance, adds to its vulnerability to
discovery by the SA of the true nature of the resemblance. T h e resulting negative
selective consequences for the mimic have been responsible, in many cases, for
the evolution of redundant adaptations such as secondary defences in cryptic and
aposematic resemblers (as well as aposematic organisms not involved in ARs)
and escape at the population level via selection for aspect diversity (individual
variability and polymorphism), again most characteristically seen in the types of
AR just mentioned.
The validity of the AR concept is supported by evidence for the significance of
the distinction between resemblances and their specifics. Examples of this kind of
evidence include: distributions of mimetic and non-mimetic morphs of
polymorphic taxa which coincide with distributions of models and areas from
which models are absent, respectively, as described in the cases of North
American species of the butterfly genus Limenitis (Platt & Brower, 1968; Platt,
1983) and the African butterfly Papilio durdunus Brown (Wickler, 1968), to cite
two examples (see also Sweet, 1985); mimicry of the same class of models by a
variety of organisms, as may be seen among those that resemble bird-droppings,
including various insects, arachnids and at least one species of frog (Owen, 1980;
Gray, 1990; Keeton & Gould, 1986: 872, fig. 33.28, photo by E. S. Ross of an
unidentified hylid frog from Ecuador), or the innumerable examples of insects,
and not a few frogs and toads, as well as other animals, that resemble fallen dead
leaves (Cott, 1940; Wickler, 1968; Owen, 1980); the wide range in degree of
similarity among organisms involved in complex synaposematic systems, such as
those illustrated by Pappageorgis (1975).
The almost limitless variation and diversity that characterize AR are reflected
in the burgeoning glossary that has arisen from new examples and continuing
studies of previously described systems and established explanations for them.
The inclusive concept of AR draws this diversity together by providing a
common thread: the adaptive significance of resemblance per se, which
encourages ‘mimicologists’ to look for similarities, as well as distinctions, among
the multitude of cryptic and sematic resemblances that are known or yet to be
discovered. The dynamic and fascinating nature of the field of ‘mimicology’
(ARology!) is enhanced by the transitional and intermediate cases which
challenge understanding of the long established distinctions such as those
between cryptic and sematic resemblances, Batesian and Mullerian mimics (VS
Batesian and Mullerian mimicries-see Rothschild, 1979), and procryptic and
anticryptic functions. ‘The continuing race between mimic and SA to reduce the
effectiveness of each other’s ‘devices’ initially allows an observer only a single
stop-frame view of a dynamic relationship that in its early stages might not even
3 I4
A. STARRETT
be recognized. The more that is learned about almost any specific AR, the more
complex and interesting it becomes. As witness, three of the most widely known
and quoted cases involving AR have been shown through the results of
continued studies to be much more complicated and involved than was thought
when they were first described: industrial melanism (Brakefield, 1987; Sargent,
1990), differential predation on colour morphs of snails of the genus Cepuea
(Jones, Keith & Rawlings, 1977) and the monarch butterfly mimicry complex
(Brower, 1992). A continuous spectrum of adaptive resemblances may, in fact,
exist even though the distinctions among categorical groupings of resemblances
are significant and theoretically justifiable. There are more than enough new
discoveries to be made and questions to ask concerning existing cases of AR to
keep current participants in the field entertained indefinitely and to guarantee
recruitment of new investigators into the ranks.
ACKNOWLEDGEMENTS
Dr William R. Boarmarin was the first to encourage me to develop my ideas
for possible publication and Dr Paul R . Neal was instrumental, by his
enthusiasm and his own ideas and stimulating discussions, in convincing me to
bring them together in written form. Jeffrey A. Smallwood contributed
considerable time and energy organizing and computerizing the impressive
bibliography which has been accumulated over the years (and continues to
grow). Drs David W. Behrens, John A. Endler, Charles L. Hogue, Paul
R . Neal, Miriam Rothschild and four anonymous reviewers read various
versions of the manuscript and provided valuable comments, criticisms and
suggestions. T o all mentioned I here express my appreciation. I offer also
additional special gratitude to Dr Neal and Dr Rothschild for encouragement,
positive feedback and valuable insights proffered along the way.
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