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The origin and evolution of the rattlesnake rattle: misdirection, clarification, theory, and progress

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The concept of homology provides researchers with a powerful tool for interpreting evolutionary transformations; however, novel phenotypes (morphology, behavior) that lack clear homologues present unique problems. These special cases often have ambiguous adaptive histories, and evolutionary scenarios that only concern their present-day function/s may bypass important evolutionary stages. Fortunately, in these circumstances, integrative comparative methods often yield insights to possible incipient conditions. The rattlesnake rattle has long been one such evolutionary enigma owing to the fact that its structural and functional uniqueness limits the utility of homology. Consequently, its evolutionary origin and function/s has been the subject of conjecture and debate. Advances in our understanding of the origin of the rattle, unfortunately, have been stifled by a hastily reached consensus in the literature that favors the most-parsimonious hypothesis about the rattle’s origin. According to this viewpoint the rattle is believed to have had its origin in a strict defensive context (aposematic function) and subsequently evolved under the adaptive influence of an uninterrupted defensive function. On close inspection, this hypothesis does not convincingly address selection acting on the incipient stages of the rattle and fails to address the adaptive history of the style, matrix, specialized tail muscle anatomy/physiology, and behavior. Here, we address a number of claims in the literature on rattle evolution. Our goal is to contribute counterarguments to dubious assertions to a) promote a more modern and nuanced approach to the study of the origin and evolution of the rattle as an integrated organ system; and b) synthesize available evidence concerning the origin of this unique structure into a theoretical framework that eliminates explanatory gaps concerning the incipient evolutionary stages.
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e Origin and Evolution of the Rattlesnake Rattle:
Misdirection, Clarication, eory, and Progress
Randall S. Reiserer1 and Gordon W. Schuett1, 2 , 3
1e Copperhead Institute
Spartanburg, South Carolina 29304, USA.
2Department of Biology and Neuroscience Institute
Georgia State University
Atlanta, Georgia 30303, USA.
3 Chiricahua Desert Museum
Rodeo, New Mexico 88056, USA.
Correspondence
Randall S. Reiserer
E-mail: rreiserer@gmail.com
Web: www.copperheadinstitute.org
Gordon W. Schuett
E-mail: gwschuett@yahoo.com
Web: www.copperheadinstitute.org
False facts are highly injurious to the progress of science,
for they often endure long; but false views,
if supported by some evidence, do little harm,
for every one takes a salutary pleasure
in proving their falseness.
-Charles Darwin
e concept of homology provides researchers with a powerful tool for interpreting evolutionary transformations;
however, novel phenotypes (morphology, behavior) that lack clear homologues present unique problems. ese spe-
cial cases often have ambiguous adaptive histories, and evolutionary scenarios that only concern their present-day
function/s may bypass important evolutionary stages. Fortunately, in these circumstances, integrative comparative
methods often yield insights to possible incipient conditions. e rattlesnake rattle has long been one such evolu-
tionary enigma owing to the fact that its structural and functional uniqueness limits the utility of homology. Conse-
quently, its evolutionary origin and function/s has been the subject of conjecture and debate.
Advances in our understanding of the origin of the rattle, unfortunately, have been stied by a hastily reached con-
sensus in the literature that favors the most-parsimonious hypothesis about the rattle’s origin. According to this view-
point the rattle is believed to have had its origin in a strict defensive context (aposematic function) and subsequently
evolved under the adaptive inuence of an uninterrupted defensive function. On close inspection, this hypothesis
does not convincingly address selection acting on the insipient stages of the rattle and fails to address the adaptive
history of the style, matrix, specialized tail muscle anatomy/physiology, and behavior.
Here, we address a number of claims in the literature on rattle evolution. Our goal is to contribute counterarguments
to dubious assertions to a) promote a more modern and nuanced approach to the study of the origin and evolution
of the rattle as an integrated organ system; and b) synthesize available evidence concerning the origin of this unique
structure into a theoretical framework that eliminates explanatory gaps concerning the incipient evolutionary stages.
247
Introduction
e origins of evolutionary novelties are often deeply puzzling. ey are
generally associated with new functions that were absent in ancestors.
- Günter P. Wagner (2015)
We subscribe to the idea that “homology thinking” (see Ereshef-
sky, 2012) is based on three perspectives: 1) multicellular organisms
consist of developmentally individualized parts or sub-systems; 2)
developmental individuation entails evolutionary individuation;
and 3) individuated body parts are inherited, though indirectly, and
form lineages that are recognized as homologies (Wagner, 2016, p.
3). e concept of homology provides researchers with a powerful
tool for exploring and interpreting evolutionary transformations
(Mayr, 1960, 1963), and is indispensible in the elds of develop-
ment and phylogenetic systematics (Carroll, 2008; Wagner, 2015,
2016). However, novel phenotypes (morphology, behavior) that lack
clear homologues present unique problems (Moczek, 2008; Kaji et
al., 2016). Such cases often have complex adaptive histories; conse-
quently, evolutionary scenarios based only on present function/s may
overlook early evolutionary stages (Gould and Vrba, 1982; Futuyma,
1998; Carroll, 2008; Wagner, 2015). Fortunately, integrative com-
parative methods often provide invaluable insights to such enigmatic
systems in biology. Few would dispute that the rattlesnake rattle has
been one of those enigmas. e structural and functional uniqueness
of the rattle limits the utility of homology. Consequently, its evo-
lutionary origin has been the subject of conjecture and debate (see
Meik and Schuett, this volume, Rattle Evo-Devo).
The rattle of rattlesnakes is arguably one of the most com-
plex and unique natural sound-producing structures known
to science (Zimmerman and Pope, 1948; Klauber, 1972;
Meik and Schuett, this volume, Rattle Evo-Devo). The vis-
ible rattle itself is a multi-segmented set of interlocking reso-
nators that has no parallel among bioacoustic organs. As an
integrative system, the rattle combines complex morphologi-
cal (Zimmerman and Pope, 1948; Klauber, 1972; Meik and
Pires-daSilva, 2009), physiological (Conley and Lindstedt,
1996, 2002) and behavioral (Greene, 1988, 1997) character-
istics that appear highly unlikely to have evolved in a single
evolutionary step (per Gould, 2002). Accordingly, details of
the rattle’s origin (RO) and evolutionary development will
likely contribute to our general understanding of and appre-
ciation for evolutionary novelties (Carroll, 2008; Meik and
Schuett, this volume, Rattle Evo-Devo).
Unfortunately, advances in our understanding of RO have
been stied by a hastily reached consensus in the literature that
favors the most parsimonious conjecture about the rattle—that
it had its origin in a strict defensive context and subsequently
evolved under the adaptive inuence of an uninterrupted de-
fensive function. On close inspection, this hypothesis, while
perhaps broadly accurate for the origin of aposematic function,
does not convincingly address selection acting on the incipient
stages of the rattle, as noted by Schuett et al. (1984) and Sisk
and Jackson (1997). Also, it fails to address the adaptive history
of the style, matrix, specialized tail muscle anatomy, physiology,
and behavior.
248
e presumptive parsimonious explanation for RO—the apo-
sematic hypothesis—has prevailed in the literature despite a lack of
strong evidence in its favor. Some authors have posited a distrac-
tive function for defensive tail vibration, even the rattle itself (Wil-
liams, 1966, p. 231), yet tail injury appears to be uncommon in
pitvipers, presumably because these snakes are dangerous and their
tail-vibration displays are associated with a defensive posture that
presents an eective deterrent (a venomous strike) to tail-biting.
us, unlike “defenseless” snakes (Willis et al., 1982), predators do
not often get the opportunity to bite the tails of rattlesnakes and
viperids (but see Schuett et al., 1984; Fathinia et al., 2015).
Here, we address a number of claims in the literature on rattle
evolution. Our primary goal is to contribute counterarguments to
assertions that have been perpetuated without careful scrutiny (see
Young, 2003, p. 314; Ernst and Ernst, 2011, p. 248; Setser et al.,
2011, p. 334) and to promote a modern and nuanced theory of the
origin and evolution of the rattle organ system (Meik and Schuett,
this volume, Rattle Evo-Devo). We present details of a theoreti-
cal model that incorporates evidence-based data on comparative
and theoretical disciplines, and accordingly propose an adaptive
scenario for the origin of the rattle.
Background
Evolutionary context for rattle evolution
Some of our best clues about causal adaptive influences on
the incipient rattle come from what we can infer about the
phylogenetic, geographic, and ecological contexts of early
rattlesnakes and their ancestral forms (Greene, 1992). Some
of these inferences are better supported than others. From
multiple phylogenetic studies (Kraus et al., 1996; Parkinson,
1999; Gutberlet and Harvey, 2002, 2004; Castoe and Par-
kinson, 2006; Fenwick, 2012; see Wüster, this volume, Phy-
logeny), we can be confident that the rattle evolved in an Ag-
kistrodon-like New World pitviper that very likely displayed
the following behavioral and morphological characters: (a)
defensive tail thrashing and vibration (Greene, 1988, 1992,
1997), (b) presence of caudal luring with contrasting tail col-
oration (Greene, 1992; Rabatsky, 2008), (c) heavy reliance on
ambush predation (Greene, 1992, 1997; Nowak et al., 2009),
and (d) a broad diet with ectothermic prey, including inverte-
brates, important to neonates (Greene, 1992, 1997; Martins
et al., 2002; Campbell and Lamar, 2004). We will argue that
each of these well-established factors played a key role in the
evolution of the rattle.
e geographic context of and ecological setting for the origin
and evolution of rattlesnakes—and hence the rattle itself—has
been largely based on speculation promulgated in the literature
for the past 75 years (Setser et al., 2011, p. 334). Uncertainty
about and incomplete information on rattlesnake relationships
has exacerbated this viewpoint (Meik and Schuett, this volume,
Rattle Evo-Devo; see Wüster, this volume, Phylogeny). Since the
late 19th century, proposals placed the origin of rattlesnakes in
the plains of North America, postulating that the rattle evolved
as a warning device to alert large animals such as ungulates (Hay,
1887; Garman, 1889; Barbour, 1922). is hypothesis has been
249
criticized for several serious shortcomings, chiey that it fails to
account for the incipient stages of the rattle—which was likely a
small structure with minimal capacity to alert ungulates (Schuett
et al., 1984; Sisk and Jackson, 1997; see paper on low levels of
defensive behavior of Sistrurus miliarius; Glaudas et al., 2005).
Fifty years later a popular proposal placed the origin of rattle-
snakes in the highlands of Mexico, mostly because high species
diversity favored that interpretation (Gloyd, 1940; see Campbell
and Lamar, 2004).
Yet another 50 years would pass before additional viewpoints on
rattlesnake origins were presented by Harry Greene (Greene, 1992,
1997) in which he hypothesized that medium-sized predators, like
Coatimundi (Nasua sp.), might easily hear the diminutive rattle of
a talus-dwelling ancestral rattlesnake in the highlands of Mexico.
is hypothesis rested partially on the classication of rattlesnakes
at the time (Klauber, 1972), which assumed that the Mexican spe-
cies (Crotalus ravus) was a member of the genus Sistrurus, based pri-
marily on enlarged head scutes. Such scutes are present in taxa (e.g.,
Agkistrodon, Gloydius) that are hypothesized to be close relatives of
the most-recent common ancestors to rattlesnakes. e taxonomic
assumption about the basal position of C. ravus has been rejected
owing to modern DNA-based phylogenetic analyses (Murphy et
al., 2002; Castoe and Parkinson, 2006; Reyes-Velasco et al., 2013).
Rather, extant members of Agkistrodon (the sister group to rattle-
snakes) and Sistrurus are distributed largely outside of the Mexican
highlands (Campbell and Lamar, 2004; Setser et al., 2011), and
the oldest fossil rattlesnake (a Pygmy Rattlesnake, Sistrurus mili-
arius), is reported from Miocene deposits (ca. 9 mya) in Nebraska
(Parmley and Holman, 2007). Consequently, the evidence assessed
thus far from the distribution of species and the fossil record does
not strongly support a Mexican origin for rattlesnakes; rather, it
favors a northerly origin for rattlesnakes somewhere within the
continental United Stated, perhaps in temperate mixed woodland
and grassland environments (Setser et al., 2011; Meik and Schuett,
this volume, Rattle Evo-Devo). While we might prot from under-
standing more about the geographic context for rattle evolution,
the behavioral context is potentially more informative for recon-
structing sources of selection on the early rattle (Meik and Schuett,
this volume, Rattle Evo-Devo).
From what we can condently reconstruct concerning the tail
behavior of proto-rattlesnakes, there are two context specic be-
haviors that likely formed the basis for early selection on the rattle:
1. Defensive Tail Vibration and rashing (DTVT). is is a
widely occurring behavior in snakes and a plesiomorphic char-
acter in rattlesnakes. It is thought to function either as an apo-
sematic display in warning potential predators, or for diverting
the attention of an attacking predator away from the vulnerable
head (Garman, 1889; Williams, 1966; Greene, 1988, 1997).
Emitting musk (“musking”) during DTVT is not uncommon
in rattlesnakes (Greene, 1988).
2. Caudal Luring (CL). is is a mimetic (deceptive) behavior
that occurs in many snake taxa, and it is particularly preva-
lent in viperids. It is typically associated with juvenile feeding
in which a prey animal (e.g., lizards, anurans) is attracted by
250
means of a moving tail that mimics the potential prey of an-
other animal (e.g., insect larva, worm). Tail-biting has been
observed in CL interactions in viperids (Schuett et al., 1984;
Reiserer, 2002; Fathinia et al., 2015; R. Reiserer and G.
Schuett, unpubl. data), and it has been hypothesized to have
played a role in rattle evolution (Schuett et al., 1984).
Tail behavior is an obvious (necessary) contender for sources of
selection on the proto-rattle, but other factors must be considered
to have an important role. Defensive capabilities, coupled with a
venom delivery system, probably set the evolutionary stage for sig-
naling displays, which provided the context for honest defensive
signals. Caudal luring is strongly associated with ambush preda-
tion, but the heavy bodies of ambush foragers limit escape strate-
gies and, thus, should also provide selective context for warning
behavior. Heavy reliance as juveniles on insectivorous, ectothermic
prey should enhance selection for mimetic tail displays that resem-
ble a “caterpillar” (or other types of insect larvae) or generalized
worm (see below). Ambivalence about the context for rattle evolu-
tion need not stie progress. Where both mimetic and warning
signals are present, we should expect to nd evidence for selection
from both in the evolution of functional morphology.
Caudal luring hypothesis for the
origin of the rattle
In 1984, Gordon Schuett and colleagues (Schuett et al., 1984)
published a brief note in Animal Behaviour on CL (feeding mim-
icry) and the origin of the rattle in rattlesnakes. Unfortunately,
the economy required by the article format prevented a detailed
discussion of the ideas put forward. Schuett et al. (1984) had
observed and lmed CL and predator-prey interactions in neo-
nates of the Eastern Massasauga (Sistrurus catenatus) presented
with newly-metamorphosed ranid frogs. During these observa-
tions, the frogs sometimes bit and attempted to swallow the tail-
tips of the luring snakes before being struck. ese observations
provided the rst evidence that tail injuries in snakes might result
from prey animals being lured. Tail-biting by prey during CL has
been conrmed in juveniles of the Copperhead (Agkistrodon con-
tortrix) and Eastern Massasauga (S. catenatus) with no noticeable
injuries reported, but recent work on adult Spider-tailed Vipers
(Pseudocerastes urararchnoidea) has documented repeated tail bit-
ing and damage to the lure by its duped prey—primarily birds
(Fathinia et al., 2015) (Figure 1).
Figure 1. e Spider-tailed Viper (Pseudocerastes urarachnoides) from
western Iran (in situ). Note the elaborate tail (caudal lure) from which
it derives its names (Bostanchi et al., 2006; Fathinia et al., 2015).
To watch this species lure birds, go to https://www.youtube.com/
watch?v=VvNrOVf17Es. Photo by Frank Deschandol.
251
Importantly, it was clear to Schuett and colleagues that the
rattle button was an integral part of the mimetic display in neo-
nates of S. catenatus, and that mimicry itself might have been
an early evolutionary driver for phenotypic change involving the
enlargement and reshaping of the terminal scale in proto-rattle-
snakes.  e caudal luring hypothesis (CLH) argues that the early
evolution of the terminal scute of proto-rattlesnakes resulted
from selection for tails that better mimicked a cephalized region
of a moth or beetle larva (Figure 2). Furthermore, increased du-
rability of a robust tail-tip and detachability, especially at a later
stage would, in theory, provide advantages related to tail injury
during CL interactions (Figure 3). Other species of rattlesnakes
that employ caudal luring include the Rock Rattlesnake (Crotalus
lepidus) and Ridgenose Rattlesnake (Crotalus willardi) (Figure 4);
Figure 2. As neonates and juveniles, some species of rattlesnakes possess a tail (caudal lure) closely resembling insect larvae or “grubs” (see references in
Schuett et al., 1984; Reiserer, 2002; Rabatsky, 2008; Reiserer and Schuett, 2008; Clark et al., 2016, www.youtube.com/watch?v=N2Nf8uMOZ2c). a) A
young Western Massasauga (Sistrurus tergeminus). b) Note the resemblance of the tail to the insect larva. c) A newborn Sidewinder (Crotalus cerastes). d) Note
the resemblance of the tail to the insect larva. Photo of Sidewinder by Ed Cassano.
AB
CD
252
CL occurs in other species of Crotalus (mostly montane taxa from
Mexico), but these accounts have yet to be published (J. Jones,
pers. comm.).
History of a debate
e earliest hypotheses on the origin and function of the rattle
(Hay, 1887; Garman, 1889; Barbour, 1922; Williams, 1966), for
whatever reason/s, generated little debate among biologists. Simi-
larly, more than a decade passed before debate commenced over
the proposals made by Schuett et al. (1984). During the 1980s
and 1990s, the ideas of persuasive gures in herpetology domi-
nated hypotheses on rattle origins. In particular, the Mexican Pla-
teau was (and remains) widely believed to be the place-of-origin
for rattlesnakes (see Setser et al., 2011; see Meik and Schuett,
this volume, Rattle Evo-Devo). In 1997, nearly 13 years after the
Schuett et al. (1984) publication, two evocative papers emerged.
One by Sisk and Jackson (1997) was a scholarly test of certain al-
ternative hypotheses of rattle origins. e other paper by Tiebout
(1997) was a awed argument, based on dubious observations
and faulty logic that criticized the CLH of Schuett et al. (1984).
e latter has been cited many times with no critical evaluation
of its arguments (see below).
In May 2000, a viper biology conference was held in Uppsala,
Sweden (Schuett et al., 2002). Many of the professional gures
interested in the controversy over the possible role of CL in rattle
origins were present at informally organized discussions follow-
ing presentations that addressed the controversy, which at that
time was recent (e.g., Sisk and Jackson, 1997; Tiebout, 1997).
In those discussions, clarication of the position held by Schuett
et al. (1984) was oered by Schuett himself, but substantially
forgotten or ignored in subsequent publications by these authors
and their students.
CLH and a straw man emerges
A pervasive misrepresentation of the CLH for the rattle’s origin
(Schuett et al., 1984) has gained unfortunate momentum (prom-
ulgation) in the literature. Certain authors have maintained that
the CLH involves a mimetic role for segment retention (SR) in
the rattle. Schuett et al. (1984) did state (p. 626) that “the rattle’s
keratinous and segmented nature may have increased the tail’s
optical attractiveness to insectivorous predators . . .” And by this
Figure 3. e yellow tail of a young Pigmy Rattlesnake (Sistrurus mili-
arius) from Florida. Note the scrapes and missing scales on the ventral
side. e photographer told us, “Based on the damaged scales, looks
like the tail got some use as a caudal lure.” See paper by Sisk and Jack-
son (1997). Rabatsky (2008) provides a review. Photo by Ed Cassano.
253
wording, certain uninformed authors (e.g., Tiebout, 1997) might
be pardoned for assuming SR involvement in the CLH. Un-
like many informed authors, however, Sisk and Jackson (1997)
did not misrepresent nor distort the CLH.  ey recognized that
scholarly tests of alternative hypotheses applicable to the origin
of the rattle must focus on the incipient stages (Schuett et al.,
1984), not functional rattles that retain segments, as presumed
by others (Tiebout, 1997; Rowe et al., 2002; Rabatsky and Wa-
terman, 2005; Rabatsky, 2008a). For clarity, “segmented na-
ture” refers to the appearance of segmentation rendered by an
un-lobed, head-like, terminal scale, which is further emphasized
by the development of constrictions (bilobation; Garman, 1889;
Sisk and Jackson, 1997) in the keratinous tail terminus (and
con gurational changes in the matrix itself) that eventually al-
lowed SR in the proto-rattle (G. Schuett, disclosure at the 2000,
Biology of the Vipers conference). All other interpretations rep-
resent a straw man that encourages  awed tests of the CLH, ob-
fuscates the meaning of the term “incipient rattle,” and hinders
real scienti c progress toward a robust and testable theory for the
origin and evolution of the rattles of rattlesnakes.
A weak foundation for rattle
evolution
While we lament the need for criticism, we recognize the neces-
sity to demolish a faulty foundation in order to renew interest in
and lay the groundwork for a robust theory on the origin of the
rattlesnake rattle. Numerous publications have addressed the hy-
Figure 4. Species of rattlesnakes that hunt by caudal luring. a) Newborn
Ridgenose Rattlesnakes (Crotalus willardi) with their putative mother,
from Arizona. Note that the tail is o -white. See paper by Schuett et al.
(1984). Photo by Brendan O’Connor. b) A newborn Rock Rattlesnake
(Crotalus lepidus), from Arizona. Note the bright yellow tail. See paper
by Kau eld (1943). Photo by Martin J. Feldner.
A
B
254
potheses of RO, but we have chosen to critique those that seem to
have most negatively impacted theoretical ideas and aected the
progress of research on this topic.
An atypical case among publications on RO is an innovative
paper that helped spark the ongoing debate. e work of Sisk and
Jackson (1997) represents a serious and scholarly attempt to test
alternative hypotheses for RO, yet there are hints of bias against
the CLH in this paper. For example, their short discussion of the
CLH focused on dismissing potential criticisms, while a longer
discussion of their falsied Dual Contact Hypothesis (DCH) fo-
cused on ways to rescue that idea. Likewise, their discussion of
future research focused on aws in the test of their preferred hy-
pothesis (DCH), and not on aws or incompleteness of their test
of the CLH. We feel the major weakness in the Sisk and Jackson
(1997) experimental design was that they tested only one species
of lizard (Sceloporus undulatus) as a dupe for their mechanical
luring experiments. Such a test is hardly robust (see Reiserer and
Schuett, 2008) and should be treated with due skepticism, yet
this study has been cited as a refutation of the CLH (Rowe et
al., 2002; Setser et al., 2011). ere is considerable variation in
the lures and luring displays of snakes, as well as the responses
of potential prey species to dierent displays (see Reiserer, 2002;
Reiserer and Schuett, 2008; Hagman et al., 2008). More rigor-
ous studies that test many dierent species are needed to gain an
understanding of potential responses to dierent tail morpholo-
gies (Reiserer, 2002; Reiserer and Schuett, 2008). e admirable
work of Sisk and Jackson (1997) is, therefore, not a refutation of
the CLH.
e report by Tiebout (1997) of putative CL in Pantherophis
alleghaniensis (formerly Elaphe obsoletus, see Crother et al., 2012),
has little to do with the origin of the rattle; yet despite its many
aws, the ill-informed and speculative discussion therein has been
cited as evidence against the CLH (e.g., Moon, 2001; Young,
2003). Tiebout regarded his observation as preliminary, but it
should be viewed as dubious. e behavior he observed never
actually lured a lizard. His conclusions are based on a single aber-
rant individual from a single clutch observed under conditions
that were not controlled. e snake was 5.5-months-old when
the behavior was rst observed, but size data were not reported
for this subject. e luring-like behavior occurred just four times
over a short period of time, and it always followed unsuccessful
pursuit of the prey. Some trials involved stalking without CL-like
behavior. Furthermore, it was not stated whether the snake as-
sumed a coiled posture (a sign of stereotypy) during tail displays.
Indeed, it seems likely it did not, given that Tiebout (1997) re-
lates two positions for the wiggling tail and that the snake re-
sumed stalking behavior after tail wiggling in some instances.
Mullin (1999) later described caudal distraction in P. al-
leghaniensis and recognized that it was distinct from CL. Our
conclusion about Tiebout (1997) is that the behavior he observed
and reported on did not meet the denitional criteria (require-
ments) for CL (Strimple, 1992). At best, what Tiebout reported
on was unsuccessful instances of caudal distraction (see also Mur-
ray et al., 1991 for another likely case of distraction mistaken
for CL in the limbless geckonid, Lialis burtonis). Unfortunately,
the dubious claim of CL in P. alleghaniensis by Tiebout (1997)
255
has been promulgated in the herpetological literature, and it has
played a role in obscuring details of phylogenetic pattern and be-
havioral features of CL (as did Murray et al., 1991). Worse yet,
Tiebout leveraged his observation to engage in speculation about
the origin of the rattle. He asserted that three lines of reasoning
argue against the CLH: (a) no incipient rattle-like structures have
evolved in other snakes that lure, (b) the incipient rattle might
have enhanced sound production or prevented wear to the tail
tip, and (c) segmented rattles appear not to be used in CL and
may diminish its eectiveness.
We maintain that each of these three arguments (conclusions) is
fallacious and has serious aws which have been overlooked, even
by one of us (Reiserer, 2002). e rst argument conated evolu-
tionary novelties (rare and unique) with evolutionary convergences
(somewhat common owing to similar selection acting on homolo-
gous structures). e second contention was partly refuted by ex-
perimental evidence the same year (Sisk and Jackson, 1997), and
there is no evidence whatsoever that erosion by friction (“wear”)
plays a role in selection on the vibrating tails of pitvipers or any
other snake taxa. Furthermore, the internal remodeling of bone
and tissue involved in rattle development has nothing to do with
abrasion or sound production, though it could help defend against
tail injury from biting. e matrix and style are novel internal
structures associated with the development, support, and muscle
attachments of the specialized tail terminus in rattlesnakes. Finally,
the third line of reasoning was pure speculation at the time. Sub-
sequent research indicates that rattle length does not correlate with
luring success in S. miliarius (Rowe et al., 2002; Rabatsky, 2008)
and, while this nding has been interpreted as a refutation of the
CLH, it is certainly not one. e nding that rattle extension does
not diminish luring success (see Rabatsky, 2008) actually supports
the CLH. Indeed, sound might play a role in CL when a free rattle
segment is present (Reiserer and Schuett, 2008, p. 88).
Tiebout (1997) seems to have erected the straw man of SR,
but others have perpetuated it. For example, despite explicit clari-
cation, Rowe et al. (2002) used their data on rattle lengths in S.
miliarius to argue against the CLH. eir paper clearly indicates
that they understood that Schuett et al. (1984) was referring to
an incipient proto-rattle (Rowe et al., 2002, see p. 386 and pp.
398399), not a well-developed, segmented rattle, but this fact
seems unclear to others who read their work. Unfortunately, we
have criticisms of other points in Rowe et al. (2002), and these
bear on the topic of rattle evolution. ese authors attempted
to support the hypothesis that the rattle of S. miliarius is cur-
rently under relaxed selection and is becoming vestigialized. is
is disconcerting, because one of them (MPR) supported a very
dierent view in an earlier paper (Cook et al., 1994). In that pub-
lication, the authors posited that there was possible selection for
small tails because they were able to demonstrate a signicant de-
viation from allometric scaling in rattle size, loudness, and pitch
in S. miliarius. e views of Cook et al. (1994) and Rowe et al.
(2002) are mutually exclusive hypotheses.
We have found sample size problems in Rowe et al. (2002)
that aect important conclusions concerning allometric scaling
of rattle size and rattle loss (see Figure 11 and allometric artifact
256
discussion, p. 395). Specically, when we removed C. stejnegeri
(n = 4) and C. transversus (n = 3) from their data set, a signicant
correlation emerged (Pearson’s correlation: r = - 0.4933, n = 18,
P = 0.037). ese authors attempted to dismiss Klauber’s (1940,
1972) assessment of interspecic dierences in rattle loss based
on their non-signicant trend between rattle loss and rattle size,
which they claim (p. 395) “is driven by the high rate of being
rattleless in S. miliarius.” Given a pragmatic reassessment of their
data and methods, we nd no basis for their conclusion that S.
miliarius is under relaxed selection for rattle SR, nor for their
claim that S. miliarius be included among the rattleless rattle-
snakes (Shaw, 1964; Klauber, 1972; Radclie and Maslin, 1975).
Rather, we found evidence in their own data set for a signi-
cant allometric relationship that aects rattle retention in smaller
species. Again, we suggest that a more careful analysis is needed
to distinguish between the two mutually exclusive conclusions
reached by Cook et al. (1994) and Rowe et al. (2002).
Following the lead of Tiebout (1997) and Rowe et al. (2002),
other researchers adopted the straw man argument against the
CLH as illustrated by the following quote from Rabatsky and
Waterman (2005a, p. 90): “Schuett et al. (1984) suggested that
increasing segmentation of the tail may have enhanced the op-
tical attractiveness of the lure... is implies that adult snakes
caudal lure and that adults, who have more time to accumulate
segments, may be more eective in attracting prey when caudal
luring.” In another publication, Rabatsky (2008) specically set
out to address whether rattle SR inuenced the evolution of the
rattle. Not only was this paper founded on the straw man of SR,
but it (a) failed to provide an unbiased, critical analysis of the
literature (e.g., concerning Murray et al., 1991; Tiebout, 1997),
(b) neglected key pieces of available literature (Bostanchi et al.,
2006), (c) failed to acknowledge the ndings of cited literature
(Reiserer 2002; Reiserer and Schuett, 2008), (d) ignored specic
warnings about methods (Strimple, 1992; Reiserer, 2002), and
(e) provided a biased interpretation of data that were published.
Among the errors, for example, the following species are known
to CL from the literature, but are incorrectly coded in Rabatsky’s
(2008) table of luring species, ese include: Crotalus cerastes (Rei-
serer, 2002, missing from table), C. willardi, (Schuett et al., 1984,
miscoded), Bothrops atrox (Pycraft, 1925; miscoded, the relevant
paper is cited in the table), Bothriechis schlegelii (Antonio, 1980,
miscoded), Proatheris superciliaris (Morgan, 1990, missing from
table), Vipera latastei (Parellada and Santos, 2002, missing from
table), three species of Atheris (Pook, 1990; Emmrich, 1997, miss-
ing from table), and others. Despite its obvious aws, the results
presented in this paper have been cited as providing evidence that
CLH is not supported (see Ernst and Ernst, 2011, p. 248).
Another study that falters under scrutiny is Moon (2001),
which not only recycled the three fallacious arguments of Tiebout
(1997) discussed above, but attempted to construct an argument
for a strictly aposematic origin of the rattle based on data gleaned
from two unpublished master’s theses (Forbes, 1967; Kerins,
1969). Instead of trusting raw intuitions about the values present-
ed in Moons (2001) data table, we calculated the dierences be-
tween tail and body measurements of the three physiological indi-
cators. is procedure would appear to be a minimally judicious
257
analysis. We re-plotted the raw data, and it is clear that Moons
(2001) conclusions do not follow from the data he published
(Figure 5). Indeed, a confusing story emerges when the dierent
physiological measurements are considered. Dierences in VO2
favor a physiological similarity between C. horridus and S. mili-
arius, while dierences in succinic dehydrogenase activity favor
a similarity between C. horridus and A. contortrix; dierences
in the optical density of cytochrome oxidase favor a similarity
between S. miliarius and A. contortrix. When variation (mea-
surement error?) is considered, the muscle physiology of Coluber
constrictor appears to be similar to that of A. contortrix. Taken
together these data support a muscle physiology for S. miliarius
that appears somewhat intermediate between C. horridus and A.
contortrix, but we advocate a suspension of credulity until these
experiments can be repeated. Unfortunately, tail shaker muscle
anatomy of basal rattlesnakes remains largely unexamined, yet
unwarranted speculation rides on scanty evidence (Savitzky and
Moon, 2008).
Normally, we would not comment on an unpublished manu-
script, but a relevant paper, submitted to a major journal, was
freely available online at the time of this writing. e authors
(Allf et al., in review) claim that their analysis supports a role
for behavioral plasticity in the evolution of the rattlesnake rattle.
While we could oer multiple points of contention with the
methods, assumptions, interpretations, and conclusions of this
paper, we wish only to point out that the conclusions represent
an attempt to speculate beyond what one may truly glean from
incomplete analysis of incomplete data. e paper attempts to
support the aposematic only hypothesis (e.g., defensive tail vi-
bration is the only selective inuence considered) and dismiss
the CLH with typically inconclusive arguments. Furthermore,
we argue that the conclusions of Allf et al. (in review), whether
meritorious or not, do not play a role in refuting the CLH.
Figure 5. Dierences between values for respiratory activity of mid-
body and tail muscle reported by Moon (2001). VO2 = rate of oxygen
consumption, sdh = succinic dehydrogenase, and co = cytochrome oxi-
dase (change in optical density). Moon (2001) reported raw values that
were perhaps not intuitive to reviewers, and asserted that Agkistrodon
contortrix displayed muscle oxidative capacities intermediate between
tail-rattling colubrids (Coluber constrictor) and rattlesnakes (Sistrurus
miliarius and Crotalus horridus). Plotting dierences between mid-body
and tail muscle measurements leads to a revised conclusion. Error bars
= SD calculated as the square root of the sum of variances. e cross-
hatched bar is reported here as a positive number, but would have been
negative as reported by Moon (a possible transposition).
258
In conclusion, what we can establish at this point in time is that
S. miliarius rarely uses its rattle in aposematic displays, nor can
it sustain rattling for protracted periods when compared to other
species of rattlesnakes (Rowe et al., 2002; Glaudas et al., 2005; Ra-
batsky and Waterman, 2005b), especially in the genus Crotalus (R.
Reiserer and G. Schuett, pers. observ.). is basal rattlesnake spe-
cies: (a) is not highly defensive, (b) has limited tail movements and
rattling, and (c) has a simple aposematic display relative to other
rattlesnake species (Glaudas et al., 2005). On the other hand, S.
catenatus and S. tergeminus (sister group to S. miliarius) are capable
of sustained rattling, though not like most members of the genus
Crotalus. ese three species form the basal clade of rattlesnakes;
thus, it is not clear yet whether the diminished rattling capacities
of S. miliarius are conserved or derived. We suggest that much of
the literature on the origin of the rattle is unsupported rhetoric
that falsely claims to test the CLH. It is time to adopt an evidence-
based approach to this interesting evolutionary problem, one that
makes use of comparative, behavioral, theoretical, and evo-devo
approaches to answer questions about the origin of the rattlesnake
rattle.
Building a robust theoretical
foundation to study the
evolution of the rattle
e debate about the origin of rattlesnakes and the rattle has been
largely the domain of herpetologists, many of them unfamiliar
with the theoretical and empirical strides made on aposematism
and mimicry over the past several decades. Particularly relevant to
rattle evolution, Magnus Enquist and colleagues (Enquist et al.,
2002) studied models of game theory, a powerful conceptual and
pragmatic tool for understanding strategies that emerge when in-
dividuals compete for limited resources (Maynard Smith, 1982;
see work by the late Nobel Laureate John Nash). Enquist’s team
also addressed the topic of aggressive mimicry (e.g., prey luring)
and showed that many assumptions of equilibrium models fail to
describe the interactions between species involving conicts of in-
terest, as in deceptive predatory events. Such interactions tend to
lead to evolutionary strategies that rapidly evolve out-of-equilib-
rium and result in spectacular modications of morphology and
behavior (Box 1).
ese “arms races” can be seen in the extravagant morphol-
ogy and bizarre behaviors of many species (in multiple lineages)
that include aggressive mimics, such as the Tasselled Wobbegong
(https://vimeo.com/112015035), many species of deep sea Angler-
shes (Pietsch 2009; Fenolio, 2016) and shallow-water Frogshes
(Pietsch and Grobecker, 1987), Alligator Snapping Turtles (Drum-
mond and Gordon, 1979), boids, pythonids, and viperids (Neil,
1960; Heatwole and Davison, 1976; Strimple, 1992), including a
viperid restricted to western Iran, the Spider-tailed Viper (Pseudo-
cerastes urarachnoides) that is relatively new to science (Bostanchi
et al., 2006). As already mentioned, this viperine species evolved a
bizarre-looking tail unlike any other members of its genus, which
astonishingly resembles a spider or centipede (Figure 1). When
used as a lure, the tail attracts birds, most of which are migratory
(Fatinia et al., 2015). e discovery of and studies on P. urarachnoides
259
bear on rattle evolution in that its tail is a unique evolutionary in-
novation in step with what Schuett et al. (1984) envisioned for the
incipient rattle. However, the tail of P. urarachnoides shows no sign
of developing into a rattle, nor is that an expectation in the emer-
gence and evolution of novel structures. Most important to the
discussion is that the peculiar tail of P. urarachnoides demonstrates
how mimicry can be a powerful driver of evolution. It leaves little
room for a failure-of-imagination concerning novel luring struc-
tures in snakes in view of other comparative data on the spectacu-
lar eects of mimicry on evolving morphology and behavior in so
many other animals and plants. e comparative approach is our
best laboratory—nature has elegantly done the tough experiments
in deep history.
Where we lack resolution concerning the context for rattle evo-
lution, we have much to survey through comparative studies that
oer general principles about the evolution of novel structures. For
example, when we reviewed examples of aposematism in verte-
brates, besides the rattle we could nd no examples of complex and
novel structures dedicated to defensive displays. Rather, aposematic
Game theory is a powerful tool for understanding and predicting the evolution of rational strategies that exist between individuals (Maynard Smith, 1982).
It places a strong emphasis on understanding adaptive behavior, which can be attained only at specic evolutionary equilibria (Nash equilibria). Under such
stable equilibria, no player can gain anything by using an alternative strategy. In other words, maximizing tness cannot be achieved by acting outside the
dened boundaries of the game of rational choices.
But, like any tool, game theory has its limits. In an exciting and ground-breaking paper, Magnus Enquist and his colleagues (Enquist et al., 2002) suggest
that behaviors of organisms often occur outside the scope of game theoretic analysis, mostly because many types of interactions involve conflicts of inter-
est between the players. In these cases, specic acts appear to promote the evolution of manipulative (deceptive) strategies (for reviews, see Wickler, 1968;
Jackson and Cross, 1987).
Enquist and colleagues (Enquist et al., 2002) state (p. 1585), when “…evolutionary processes are at equilibrium, predictions about behavior can be ob-
tained simply by asking what is the most profitable way to behave, without considering the dynamics of the evolutionary process ….” (see Parker, 1979,
1983; Parker and Maynard Smith, 1990; Grafen, 1991). For evolutionary change to occur, however, strategies must exist out of equilibrium for some
period of time (Maynard Smith, 1982). e extent to which persistent and wide-ranging non-equilibrium conditions occur in nature is not known, but it
is likely they are much more prevalent than previously suspected.
Box 1. Spectacular phenomena, limits to rationality, and the powerful role of deception and mimetic
resemblance in evolution
260
Another important point that Enquist and colleagues (Enquist et al., 2002) present is that equilibrium may never be attained owing to the nature of the
interaction itself. ey state (p. 1585), “When an advantageous trait evolves in one player, this can be to the disadvantage of other players, and vice versa.
is scenario may result in endless cycles of adaptation and counter-adaptation among the dierent classes of players, with the result that evolution pro-
ceeds out-of-equilibrium for much of the time, with behavioral strategies in an almost continuous state of flux ... under such conditions strategies may
emerge and persist which cannot be part of a game theoretical equilibrium. e players in such games seek to manipulate one another, and behavior evolves
that appears to be irrational when judged against optimization principles.” Furthermore, because so many interactions of organisms appear to be outside
the scope of game theory, the model that Enquist and colleagues derive challenges the view that the analysis of behavior can be achieved by the use of game
theory alone. Rather, they suggest that in many situations evolution proceeds out-of-equilibrium. Accordingly, the strategies that emerge in such games are
more appropriately viewed as staging posts on the road of an evolutionary race rather than as stable end-points predicted by game theory (Dawkins and
Krebs, 1979).
Prey luring is a deceptive act, often classied as aggressive mimicry (Wickler, 1968; Vane-Wright, 1976; Pasteur, 1982; Jackson and Cross, 2013), and it is
a classic example of a behavioral strategy that proceeds out-of-equilibrium, produces spectacular morphology, involves a player (dupe) that acts irrationally
(non-adaptively), and spreads rapidly in the population. e out-of-equilibrium model (Enquist et al., 2002) has two main predictions that are particularly
relevant to our discussion of rattle evolution.
First, it appears that manipulation (deception) and conict of interest situations are common in nature. Most cases described involve two or more dierent
species. ese include, but are not limited to, prey luring, sexual mimicry, and brood parasitism. In cases involving prey luring, it seems undisputed that
the bizarre lures and odd-shaped (exaggerated) morphologies of Frogshes, Alligator Snapping Turtles, Tasselled Wobbegong, viperid snakes, and numer-
ous other species were shaped by the mimetic (deceptive) process itself (Figure 6). In other words, mimicry is a powerful driver of morphological evolution.
Second, evolutionary change is rapid in traits used during manipulation. Interestingly, in cases of prey luring, the lure itself sometimes evolves as a near-
perfect replica of an intended model, such as sh (Pietsch and Grobecker, 1978) or a centipede (Fathinia et al., 2015).
Accordingly, given these predictions, it appears possible that the rattle organ system originated as a deceptive display, evolving out-of-equilibrium under
conditions of conict of interest, and subsequently exapted to its present role as an aposematic display.
Box 1. Continued
261
Box 1. Continued
B
D
Figure 6. Species of vertebrates that show prey-luring. a) Painted Frog sh (Antennarius pictus). b) Alligator Snapping Turtle (Macroclemmys sp.).
c) Tasselled Wobbegong (Eucrossorhinus dasypogon). d) Cottonmouth (Agkistrodon piscivorus).
A
C
262
displays are dominated by structures that have undergone chang-
es in color and pattern. In cases where they involve sound they
are associated with modications of existing structures for sound
production (e.g., Dunning and Kruger, 1995; Barber and Con-
ner, 2007). Incidentally, aposematic displays do not involve strong
(if any) conicts of interest owing to the fact that they are honest
signals to other species, whereas luring (deceptive) displays involve
the ultimate conicts of interest.
ese observations should compel us to take a closer look at ideas
about the defensive origin of the rattle. On the other hand, armored
defenses do sometimes result in complex structures (Emlen, 2014),
but these innovations generally represent exaptations of homolo-
gous structures (Gould, 2002). Despite much discussion about the
aposematic role of the rattle, we mostly lack empirical (experimen-
tal) evidence for the rattle’s aposematic role in nature. With respect
to rattling behavior, for example, most of our observations (data) of
rattlesnakes involve them responding to threats made by humans.
Rather than context, it is comparative data that provides our best ev-
idence for the aposematic role of the rattlesnake rattle. Aposematic
displays are often mimicked by other species (e.g., Burrowing Owls,
Rowe et al., 1986; Gopher Snakes, Sweet, 1985) which presum-
ably gain protection from Batesian mimicry (deception) by making
rattlesnake-like sounds and postural displays. Importantly, apose-
matism might be favored only to the extent that it allows predators
to distinguish dangerous species from innocuous ones (Sherratt and
Beatty, 2003) and, therefore, might not produce suciently strong
selection to facilitate complex structural changes, such as those that
occurred in the rattle of rattlesnakes.
Clarication of current theory
It is important to remember that the rattle owes its interlocking
nature to constrictions that form a loosely clasping, nested con-
guration involving a unique developmental process that results
in segment shifting (Zimmerman and Pope, 1948; see Meik and
Schuett, this volume, Rattle Evo-Devo). e rattle system is not a
simple structure, and it likely required a long period of evolution-
ary ne tuning. For clarity and comparison, we discuss below two
sketches of the main theories for rattle evolution. Our aim here is
to be explicit about the dierences between a purely aposematic
hypothesis for RO and one that hypothesizes a key role for mim-
icry in shaping the proto-rattle.
e sequential details outlined in this hypothesis of rattle
evolution should be considered exible, since we have not yet
determined the evolutionary order of many of the rattle’s struc-
tural features. As such, selective inuences might have arisen at
dierent times relative to each other and the structural changes
involved. Evolutionary-developmental studies will, no doubt, re-
ne the following interpretations. e goal of this theoretical ap-
proach is to lay out possible evolutionary sequences that account
for all stages (when possible) of rattle evolution under a continu-
ous series of evolutionary pressures (Figure 7).
Aposematic only hypothesis
is hypothesis posits that the rattle evolved solely in an apo-
sematic context. We know from pitviper outgroup taxa (ge-
nus Agkistrodon) that a modestly enlarged, conical tail tip scale
263
264
was likely present, which, without constrictions, was sloughed
during molts, i.e., it did not itself produce or enhance sound
(Sisk and Jackson, 1997). On aposematic theory alone, we have
no viable hypothesis for a selective advantage that might have
shaped this initial phenotype into a rattle in a stepwise fashion.
Indeed, we have empirical evidence against an aposematic role
for enlarged tail tips (Greene, 1992; Sisk and Jackson, 1997).
To rescue the aposematic hypothesis, we must minimally posit
that a proto-style and matrix rst evolved in a form that allowed
rattle segment articulation or created some unknown aposemat-
ic advantage. We grant this “hopeful monster” scenario (Gold-
schmidt, 1940) here for the sake of discussion, and acknowledge
that single-gene mutations can have large impacts on dierent
phenotypes, i.e., pleiotropic inuences (Chouard, 2010). How-
ever, it is an empirical question whether the rattle arose from a
single-gene mutation—one that has not yet been answered—
and evo-devo studies will help to answer this question (Carroll,
2008; see Meik and Schuett, this volume, Rattle Evo-Devo).
For selection to rene the proto-rattle, some aposematic ad-
vantage would need to accrue to the incipient rattle. Assuming
that the proto-rattlesnake was, unlike S. miliarius (Glaudas et al.,
2005), suciently formidable to advertise its dangerous nature,
the sudden appearance of a sounding device would presumably
provide that advantage. Until chain formation was achieved,
however, it is unclear how the incipient rattle could play a role
in aposematic signaling that produced an audible (or other) ad-
vantage over that of a thrashing prototypical tail. With a sud-
den enlargement of the tail terminus, constrictions for SR, and
segment shifting development, the nascent rattle could immedi-
Figure 7. Unbroken sequence of evolutionary stages in rattle development illustrating the caudal luring hypothesis (CLH) of the rattle’s origin. We parti-
tioned this evolutionary sequence into six conceptual stages to emphasize possible transitions of selective inuences on the incipient rattle organ system.
Mimicry dominated the incipient stages (stages 13), which rst resulted in terminal scale enlargement, followed by constriction of the end scale. Mimetic
selective forces (Box 1) increased the tail’s resemblance to a cephalized, segmented invertebrate, which also brought about changes in the generative tissue
(matrix) and its bony substratum at the apex of the tail. In our opinion, the major evolutionary transition occurred between stages 3 and 4, when a bi- or
tri-lobed end-cap, which was formerly shed during molts, gained a clasping conguration and a position shifting developmental process by which a new
proximal lobe was added anterior to the old proximal lobe from the previous ecdysis (see Meik and Schuett, this volume, Rattle Evo-Devo). is innovation
would have opened the door for sound production. Subsequently, with the advent of specialized rapid tail movements and changes in behavior, the apose-
matic role of this organ system became the dominant selective inuence (stage 5). Based on multiple lines of evidence, we suggest that early rattlesnakes had
small, relatively quiet rattles which could be deployed for only short durations (e.g., Sistrurus miliarius). Once aposematic sound production was achieved,
certain lineages evolved hyper-aposematic, multi-modal displays (stage 6) involving increased body size (formidability), large rattles and hissing (acoustic),
bold defensive postures (behavioral), starkly banded tails (black and white), larger quantities of venom per bite, and perhaps in some cases increased toxicity
(Figure 8). In reference to a purely aposematic hypothesis to account for the origin of the rattle, this model lls major theoretical gaps in selective regimes
present and acting on the early proto-rattle and incipient rattle. Namely, it adds stages 2 and 3, which provide an explanation for early and important mor-
phological changes that must have required evolutionary tinkering. e transition (gradient) in selection (mimetic to aposematic) advantage appears to be
complete in derived rattlesnakes (e.g., C. atrox), but is incomplete in those species that still employ caudal luring (Figures 24), most of which are small as
adults and have limited and less dramatic aposematic repertoires (see Eberhard, 2011).
265
ately serve as a warning to predators that learned to distinguish
this dangerous pitviper from harmless snakes. e signal would
not need to be loud or particularly stereotyped, just salient to a
particular set of common threats, whether predators or brows-
ing ungulates. us, no behavioral modications need be pos-
tulated for the early rattle. Selection could subsequently favor
renements in the tail muscles to produce a more audible signal.
However, since the shape of the rattle depends upon the shape
of the style, one must hypothesize that both the style and matrix
evolved simultaneously to produce a loosely clasping string of
segments that produced sucient sound to act as a warning. To
be clear, this hypothesis requires a rapid and global change in-
volving the simultaneous origin of style and matrix morphology,
i.e., the simultaneous origin of both osteological and integumen-
tary features, as well as a segment shifting mechanism. Without
these features, segments could not accumulate and there would
be no ability for sound production, as in Crotalus catalinensis
(Klauber, 1972).
Integrative hypothesis:
the mimicry to aposematism gradient
As in the aposematic hypothesis, early proto-rattlesnakes possessed
a modestly enlarged, conical terminal scale that was sloughed
during molts. is structure evolved in the context of both apo-
sematic tail vibration and CL—and likely selection for both. Un-
der selection for enhanced mimetic resemblance to the head of
a caterpillar-like insect (Schuett et al., 1984), this conical struc-
ture enlarged and changed shape via local changes to the stratum
granulosum and underlying bone (forming a proto-style, similar
to the terminal vertebral element seen in radiographs of P. ura-
rachnoides, Bostanchi et al., 2006). e early adaptive history of
the incipient rattle might have involved multiple behavior modes
and movement patterns, including the defensive (or distractive)
tail thrashing display used by alarmed pitvipers and other snakes,
but modern rattling movements do not resemble DTVT—there
is only a small side-to-side deection in the rattling tail and high-
speed video has revealed movements more akin to CL (distally
traveling waves) than to tail thrashing or side-to-side vibration
(information derived from the high-speed videography lab at e
Copperhead Institute, C. Smith, pers. comm.).
Another behavioral innovation associated with rattling is
that the tail is typically held aloft rather than engaged with the
substrate. is stereotyped position is also reminiscent of CL
rather than DTVT. Patterns of movement and stereotypy might
reveal much about the rattle’s evolutionary past. Likewise, color
and pattern might be informative, since they epitomize changes
associated with aposematic displays. Multi-modal aposematic
displays in crotalines predate the rattle and appear to include
components of color, pattern, sound, smell, postures, and threat
behaviors (see Greene, 1997), most of which do not involve the
tail. Aposematic tail behaviors in crotalines appear to be largely
associated with sound production that calls attention to other
aposematic display modes. With one possible exception (C. ce-
rastes), all basal rattlesnakes lack stark black and white tail band-
ing, which we view a priori as an aposematic signal (see Caro,
2009, 2013). We thus might provisionally dismiss aposematism
as the primary inuence on early rattle evolution in favor of
266
hypotheses concerning the potential advantage of an armored
structure that would resist the bites of attracted prey and per-
haps distracted predators. As previously mentioned, however,
there is little evidence that the tails of pitvipers are particularly
vulnerable to injurious attacks by predators, but there is evi-
dence for tail injuries from lured prey (Fatinia et al., 2015; see
S. miliarius image in Figure 1). With knowledge and direction
in hand, we need to be looking for evidence.
e critical evolutionary events for a functional rattle were
the appearance of constrictions in the terminal scale (Sisk and
Jackson, 1987) and the evolution of segment-shifting develop-
ment, which allowed successive exuviae to form an interlock-
ing chain (Figure 7). ese congurational changes probably
required some ne tuning before an aposematic rattle was
achieved. ere is no reason to assume that at this early stage
(stage 4, Figure 7) selection would have favored specialization
of the tail musculature for rapid and sustained vibration, nor is
there much reason to presume that a robust style had begun to
evolve via fusion of tail vertebrae. However, because the shape
of integument features appears to be associated with osteologi-
cal morphology, it seems likely that the terminal tail vertebra
underwent modication associated with shape changes (the de-
velopment of constrictions) in the incipient rattle. Under the
inuence of mimicry, a plausible Darwinian scenario unfolds
whereby the fully developed aposematic role of the rattle devel-
oped over time under selective feedback from various sources
(Figure 7). It is also reasonable to hypothesize that an early rattle
with interlocking segments produced sound during tail thrash-
ing or luring displays (Reiserer and Schuett, 2008), as observed
in S. miliarius today, but it seems unlikely that this poorly de-
veloped sound would function as a salient display for defense,
and, indeed, S. miliarius does not appear to use its rattle as an
eective aposematic display (Glaudas et al., 2005).
We know that both the CL and defensive, though not neces-
sarily aposematic, roles were present in the tail displays of the
ancestral rattlesnake. us, both of these roles are candidates for
selective inuence on the rattle. More study is needed on the ef-
fectiveness of defensive tail thrashing in other pitvipers to un-
derstand the basal condition in rattlesnakes. We know that the
aposematic role of the rattle became dominant in advanced rattle-
snakes and that CL (and tail color) was mostly lost, which is the
derived condition in rattlesnakes (R. Reiserer and G. Schuett,
unpubl. data). If the rattle had its origin as a mimetic structure,
there was a transition from a deceptive lure to warning signal that
resulted in an explosive adaptive radiation, culminating in hyper-
aposematic displays which comprise multi-modal signaling (Fig-
ure 8). For some advanced species, the transition is complete, but
for those that retain caudal luring we might expect to detect selec-
tion which still favors traits that enhance mimetic resemblance.
Summary and conclusions
e uniqueness of the rattlesnake rattle commands the meticu-
lous attention of evolutionary science—the rattle’s phenotypic
complexity persuades against a simplistic explanation of its origin.
It is tempting to adopt a parsimonious scenario for the evolution
267
of this unique structure. After all, the rattle evolved in the context
of aposematic tail vibration, as well as caudal luring, so why as-
sume that mimicry was involved at all? e most robust answer
includes the general observation that mimicry is a demonstrably
powerful driver of morphological evolution (Box 1), something
we can see in many marine shes (Pietsch and Grobecker, 1987;
Pietsch, 2009), tropical frogs (Murphy, 1976), several turtles
(Drummond and Gordon, 1979), snakes (Neil, 1960; Pough,
1988; Strimple, 1992), mollusks (Gould, 1977, pp. 103110),
and even plants (Wickler, 1968). In contrast, there is little evi-
dence from comparative analyses that aposematism is a powerful
evolutionary driver of morphological novelties (Gould, 2002).
Furthermore, scenarios of rattle evolution based on a strict role of
aposematism create unacceptable gaps in the selective processes
that must have been in operation during incipient stages of the
evolution of such a complex system (Gould, 1977, 1980, 2002;
Wagner, 2015; Kaji et al., 2016; Meik and Schuett, this volume,
Rattle Evo-Devo).
To be clear, we concede that aposematic signaling played a
continuous role in the selective history of the rattle, but we pro-
visionally reject any dogma that claims primacy for aposematism
in the evolution of the rattle. ose with an earnest interest in
resolving the evolutionary details of RO should revisit what it
means to evolve out-of-equilibrium (Enquist et al., 2002). is
process generates what Eldredge and Gould (1972; see Eldredge,
2015) detected as punctuation in the fossil record, and what En-
quist et al. (2002) modeled for deceptive displays. Directional
evolution occurs when stabilizing selection loses out to disrup-
tive forces (Mayr, 1960; Endler, 1986; Futuyma, 1998). But we
must ask ourselves whether the evidence at hand supports the ap-
parently subdued evolutionary processes for aposematic displays
(Sherratt and Beatty, 2003), or the radical phenotypic changes
associated with mimicry (Enquist et al., 2002). We maintain that
in the face of the complexity of the rattle (Zimmerman and Pope,
Figure 8. Multi-modal aposematic threat display by an iconic rattle-
snake species of the Southwest. An adult Crotalus atrox in a typical
raised posture. In addition to postural signals, such displays incorporate
sound (rattling and hissing), other visual signals (tongue arching, stark
black and white tail banding), and overt intimidation (mock strikes).
Together these signals comprise an integrated deterrent (warning) sys-
tem. Photo by Martin J. Feldner.
268
1948; Meik and Pires-daSilva, 2009; Meik and Schuett, this vol-
ume, Rattle Evo-Devo), it is unjustiable to appeal to hopeful
monster theories—we must search for and strictly rely on the
best evidence.
Acknowledgments
is chapter has been in incubation/development for more than
a decade, and there have been many people along the way who
contributed to our discussion of rattle origin and evolution, but
primarily Dave Chiszar, Harry Greene, Jason Jones, Fred Kraus,
Jesse Meik, Louis Porras, and Chuck Smith. For comments and
insights on a draft of this manuscript, we are grateful to Harry
Greene, Jesse Meik, and Charlie Radclie. However, this does
not imply they agree with any or all aspects of our proposed ideas.
Furthermore, all blunders remain our responsibility. For use of
photos we thank Ed Cassano, Frank Deschandol, and Martin
Feldner. We dedicate this work to the memory of our colleagues
and dear friends, Chuck Carpenter and Dave Chiszar. Both of
these men played an important role in mentoring us and sup-
porting our research on caudal luring in snakes—they are sorely
missed.
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... One long-standing theory for the evolution of the rattlesnake rattle is that it evolved as a warning signal to alert large grazing animals on the plains of North America (Hay 1887;Garman 1889;Barbour 1922). However, this hypothesis has been challenged by several authors (Schuett et al. 1984;Sisk and Jackson 1997;Glaudas et al. 2005;Reiserer and Schuett 2016). Although free-ranging cattle are only present at this study area for a short period of time, and generally before most snakes migrate from denning habitat to summer habitat (approximately 6 weeks from April to mid-May; Atkins 2021), during the active season, we recognize the possible confounding effect of the presence of cattle at the Ranch site in the North Okanagan study area. ...
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Frequent human encounters, even if benign, can influence fight-or-flight decisions in animals. Understanding how these responses are linked to human activity provides important insight into the ecology and conservation of populations, particularly those that may interact with humans. To this end, we compared the defensive behavior (rattling) of rattlesnake populations at two study areas containing habitats with contrasting levels of human activity. Immediately after capture in the field, we subjected rattlesnakes to the approximation of an approaching hiker and recorded the distance that they first rattled. To accommodate for zero inflation in our analysis, we developed a two-part model. We first assessed the probability of rattling occurring via a logit model, followed by a log-normal regression model to assess the distance to initiation of rattling as affected by covariates (site, temperature, time of year, snake size, etc.) for all non-zero values. Snakes occupying areas subject to high levels of human activity allowed investigators significantly closer before rattling (P < 0.001). Compared to areas of low human activity, these snakes were 6.17–7.61 times less likely to engage in rattling behavior at all. We argue that the uniform response recorded among rattlesnakes in areas of high human activity suggests population-level habituation to human presence. The behavioral differences we detected over relatively short distances have implications for land management, including the impacts of recreational areas with a high degree of human activity. Our findings are consistent with studies of other taxa on the impact of human activity on animal behavior, suggesting this pattern may be widespread. Significance statement The influence of human activity on the behaviors of wildlife is difficult to quantify but of significance for conservation and management. We studied how the defining defensive behavior of rattlesnakes, tail rattling, differs according to environmental conditions. Rattlesnakes in areas of high human activity displayed a highly uniform, muted response to an approaching investigator when compared to snakes in areas of negligible human activity. Our results suggest that the level of human activity on a landscape may influence the expression of a core behavior in rattlesnakes, and that behavioral shifts may become evident in habitats subject to contrasting levels of human activity within a relatively short period of time. With replication, this type of survey could serve as a less costly alternative to traditional population impact studies for rattlesnakes.
... We have observed skin at the abdominal (ventral) part and the tail of the Burmese Python (Python bivittatus) (Figure 10) and the lip part of the Emerald Tree Boa (Corallus caninus) (Figure 11). From the outer scale surface toward the dermis are the oberhautchen layer, β-layer, mesos layer, α-layer, lacunar layer, and the clear layer [1,24,25]. ...
... As already mentioned, loreal pits (see section titled 'Taxonomy and Systematics' of vipers) marked the origin of pitvipers, enhancing their capacity to detect prey, predators and adequate thermoregulation sites, and thereby probably contributing to their high number of extant species and wider distribution compared to the other two subfamilies of vipers. The rattle evolved only in rattlesnakes (Crotalus and Sistrurus) (Figure 1c and d) and might have evolved from defensive tail vibration and/or caudal luring for prey (Greene, 1992;Reiserer and Schuett, 2016); both behaviours were likely present in ancestral crotalines, the latter even more generally in vipers and perhaps macrostomatans (see below for more on caudal luring). Interestingly, loss of the rattle has occurred several times during subsequent rattlesnake evolution, perhaps owing to relaxed selection in the absence of predators, random genetic changes in rattle formation and other influences (e.g. ...
Chapter
Vipers are venomous snakes characterised by having two enlarged highly mobile fangs. They comprise more than 300 species belonging to the Viperidae, which in turn includes viperines (or ‘true vipers’), azemiopines and crotalines (or ‘pitvipers’). They first radiated in the Old World more than 50 million years ago and later rapidly diversified in the New World. Several interesting traits emerged during their evolutionary history, including thermosensitive loreal pits and parental care in crotalines and specialised sound production in rattlesnakes. Vipers are currently found in almost every available habitat on earth and occupy diverse ecological niches. Ancestrally, they evolved the ability to eat unusually heavy, bulky prey and exhibit an impressive range of diet specialisations. Although vipers represent an interesting and successful radiation, many species are threatened with extinction and several aspects of their evolutionary history still need investigation.
Article
The estimation of one’s distance to a potential threat is essential for any animal’s survival. Rattlesnakes inform about their presence by generating acoustic broadband rattling sounds.¹ Rattlesnakes generate their acoustic signals by clashing a series of keratinous segments onto each other, which are located at the tip of their tails.1, 2, 3 Each tail shake results in a broadband sound pulse that merges into a continuous acoustic signal with fast-repeating tail shakes. This acoustic display is readily recognized by other animals⁴,⁵ and serves as an aposematic threat and warning display, likely to avoid being preyed upon.¹,⁶ The spectral properties of the rattling sound¹,³ and its dependence on the morphology and size of the rattle have been investigated for decades7, 8, 9 and carry relevant information for different receivers, including ground squirrels that encounter rattlesnakes regularly.¹⁰,¹¹ Combining visual looming stimuli with acoustic measurements, we show that rattlesnakes increase their rattling rate (up to about 40 Hz) with decreasing distance of a potential threat, reminiscent of the acoustic signals of sensors while parking a car. Rattlesnakes then abruptly switch to a higher and less variable rate of 60–100 Hz. In a virtual reality experiment, we show that this behavior systematically affects distance judgments by humans: the abrupt switch in rattling rate generates a sudden, strong percept of decreased distance which, together with the low-frequency rattling, acts as a remarkable interspecies communication signal. Video abstract Download : Download video (263MB)
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What factors influence the evolution of a heavily selected functional trait in a diverse clade? This study adopts rattlesnakes as a model group to investigate the evolutionary history of venom coagulotoxicity in the wider context of phylogenetics, natural history, and biology. Venom-induced clotting of human plasma and fibrinogen was determined and mapped onto the rattlesnake phylogenetic tree to reconstruct the evolution of coagulotoxicity across the group. Our results indicate that venom phenotype is often independent of phylogenetic relationships in rattlesnakes, suggesting the importance of diet and/or other environmental variables in driving venom evolution. Moreover, the striking inter- and intraspecific variability in venom activity on human blood highlights the considerable variability faced by physicians treating envenomation. This study is the most comprehensive effort to date to describe and characterize the evolutionary and biological aspects of coagulotoxins in rattlesnake venom. Further research at finer taxonomic levels is recommended to elucidate patterns of variation within species and lineages.
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Species of the genus Lialis are 'sit-and-wait' predators. However, an important behavioral modification was revealed in this study; initial prey escape triggered caudal luring tactics in Lialis burtonis for the recapture attempts of nearly 88% of the escaped prey. The behavior of L. burtonis in all trials involving caudal movements suggests that the movement is used both as an attractive (i.e., "lure") and as a distractive device. It is believed that the caudal movements are a normal, but occasional, part of the feeding sequence of L. burtonis. Caudal luring is described for the first time in a pygopodid, and appears to be very rare amongst lizards. The occurrence of caudal luring in L. burtonis can be interpreted as yet another example of convergent evolution between these pygopodids and snakes.
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Quantitative studies of perceptual mechanisms in vipers have focused on chemosensory tongue-flicking, in part because the prevalent sit-and-wait foraging habit provides few other clues about pre-strike prey recognition. Snakes that employ caudal luring offer a unique opportunity to quantify visual perception, and to infer cognitive functions when snakes use caudal luring, pursuit, or sit-and-wait predation depending on prey type. Stimulus control of caudal luring and other prey capture tactics were examined in four phylogenetically distant vipers: the Copperhead (Agkistrodon contortrix); the Sidewinder (Crotalus cerastes); the Massasauga (Sistrurus catenatus); and the Horned Adder (Bitis caudalis). While all four species feed on a variety of prey, the luring response of each species is evoked almost exclusively by a certain type of organism, and alternate strategies are used to capture other prey types. Feeding experiments and experimental manipulations using prey-like models suggest that these vipers readily discriminate between different types of prey through visual cues involving shape and/or movement features, and that they have evolved appropriate responses for capturing particular prey taxa. Intraspecific variation in stimulus control between populations of S. catenatus suggests that evolution of perceptual mechanisms for prey recognition and appropriate response operates on a fine scale. The potential exists to understand cognitive functions, such as decision making, and the evolution of prey recognition in vipers through studies of caudal luring and differential response to prey stimuli.
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Environmentally induced behavior (behavioral plasticity) has long been hypothesized to promote the origins of novel morphological traits, but this idea remains controversial. One context in which this hypothesis can be evaluated is animal communication, where behavior and morphology are often linked. Here, we examined the evolution of one of nature's most spectacular communication signals: the rattlesnake rattle. We specifically evaluated whether rattlesnake rattling behavior-and, hence, the rattle-originated from a simple behavior: vibrating the tail when threatened. By reconstructing the ancestral state of defensive tail vibration, we show that this behavior is nearly ubiquitous in the Viperidae (the family that includes rattlesnakes) and widespread in the Colubridae (the largest snake family, nearly all of which are nonvenomous), suggesting a shared origin for the behavior between these families. After measuring tail vibration in 56 species of Viperidae and Colubridae, we show that the more closely related a species was to rattlesnakes, the more similar it was to rattlesnakes in duration and rate of tail vibration. Thus, the rattlesnake rattle might have evolved via elaboration of a simple behavior. These data thereby support the long-standing hypothesis that behavioral plasticity often precedes-and possibly instigates-the evolution of morphological novelty.
Book
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Why do elk grow majestic antlers despite the devastating costs to the rest of their bodies? Why do the crabs we see on beaches every summer frantically wave their claws at one another before engaging in battle? How are piranhas able to feed on prey so much larger than them? Every animal relies on a weapon of some kind – cats have claws, eagles have talons, even the dogs we keep as pets have a respectable set of teeth. But the overwhelming majority of these weapons stay small, proportional to the rest of the animals’ bodies. In rare cases, however, we find species whose weapons have become stunningly outsized, some with tusks or horns so massive that the males who wield them look like they should tip over or collapse under their bulk and weight. Weapons just as extreme have cropped up in walruses and narwhals, crabs, beetles, bugs and flies. What is it about these species? Why are their weapons so big? When does bigger become too big? In Animal Weapons biologist Douglas Emlen pulls readers into the worlds of these remarkable beasts, trekking through rainforests and mountain passes to unravel the mysteries of their weapons, while a series of vivid black and white drawings and gorgeous color photographs lets us marvel at them first hand. It is a journey rich with anecdotes and adventure, as well as surprises—along the way, Emlen shows that the essential biology of animal arms races applies to our own weapons, too. The same critical conditions trigger arms races in animals and in humans; analogous factors sculpt their evolution; and similar circumstances ultimately bring about collapse – the sudden, and often dramatic, end of the race. A story that begins with biology becomes the story of all weapons, as readers glide between beetles and battleships, crabs and The Cold War. Ultimately, Emlen seeks to determine where this parallel leaves us today, in a post-Cold War world filled with the deadliest weapons of all time, nuclear, biological, and chemical weapons of mass destruction.
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This book follows the development of evolutionary science over the past two hundred years. It highlights the fact that life endures even though all organisms and species are transitory or ephemeral. It goes on to explain that the extinction and evolution of species—interconnected in the web of life as “eternal ephemera”—are key concerns of evolutionary biology. The book begins in France with the naturalist Jean-Baptiste Lamarck, who in 1801 first framed the overarching question about the emergence of new species. It moves on to the Italian geologist Giambattista Brocchi who brought in ideas from geology and paleontology to expand the question. It details how, in 1825, at the University of Edinburgh, Robert Grant and Robert Jameson introduced the astounding ideas formulated by Lamarck and Brocchi to a young medical student named Charles Darwin and follows Darwin as he sets out on his voyage on the Beagle in 1831. The book revisits Darwin's early insights into evolution in South America and his later synthesis of his knowledge into the theory of the origin of species. It then considers the ideas of more recent evolutionary thinkers, such as George Gaylord Simpson, Ernst Mayr and Theodosius Dobzhansky, as well as Niles Eldredge and Steven Jay Gould, who developed the concept of punctuated equilibria. The book provides many insights into evolutionary biology, and celebrates the organic, vital relationship between scientific thinking and its subjects.