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Quantitative axial myology in two constricting snakes: Lampropeltis holbrooki and Pantherophis obsoletus

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A snake's body represents an extreme degree of elongation with immense muscle complexity. Snakes have approximately 25 different muscles on each side of the body at each vertebra. These muscles serially repeat, overlap, interconnect, and rarely insert parallel to the vertebral column. The angled muscles mean that simple measurements of anatomical cross-sectional area (ACSA, perpendicular to the long-axis of the body) serve only as proxies for the primary determinant of muscle force, physiological cross-sectional area (PCSA, area perpendicular to the muscle fibers). Here, I describe and quantify the musculature of two intraguild constrictors: kingsnakes (Lampropeltis holbrooki) and ratsnakes (Pantherophis obsoletus) whose predation performance varies considerably. Kingsnakes can produce significantly higher constriction pressures compared with ratsnakes of similar size. In both snakes, I provide qualitative descriptions, detail previously undescribed complexity, identify a new lateral muscle, and provide some of the first quantitative measures of individual muscle and whole-body PCSA. Furthermore, I compare measurements of ACSA with measurements of PCSA. There was no significant difference in PCSA of muscles between kingsnakes and ratsnakes. There is, however, a strong relationship between ACSA and PCSA measurements. I could not identify a significant difference in musculature between kingsnakes and ratsnakes that explains their different levels of constriction performance. Unmeasured components of muscle function, such as endurance and force production, might account for differences in performance between two species with similar muscle structure.
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Quantitative axial myology in two constricting snakes:
Lampropeltis holbrooki and Pantherophis obsoletus
David A. Penning
1,2
1
Department of Biology & Environmental Health, Missouri Southern State University, Joplin, MO, USA
2
Department of Biology, University of Louisiana at Lafayette, Lafayette, LA, USA
Abstract
A snake’s body represents an extreme degree of elongation with immense muscle complexity. Snakes have
approximately 25 different muscles on each side of the body at each vertebra. These muscles serially repeat,
overlap, interconnect, and rarely insert parallel to the vertebral column. The angled muscles mean that simple
measurements of anatomical cross-sectional area (ACSA, perpendicular to the long-axis of the body) serve only
as proxies for the primary determinant of muscle force, physiological cross-sectional area (PCSA, area
perpendicular to the muscle fibers). Here, I describe and quantify the musculature of two intraguild
constrictors: kingsnakes (Lampropeltis holbrooki) and ratsnakes (Pantherophis obsoletus) whose predation
performance varies considerably. Kingsnakes can produce significantly higher constriction pressures compared
with ratsnakes of similar size. In both snakes, I provide qualitative descriptions, detail previously undescribed
complexity, identify a new lateral muscle, and provide some of the first quantitative measures of individual
muscle and whole-body PCSA. Furthermore, I compare measurements of ACSA with measurements of PCSA.
There was no significant difference in PCSA of muscles between kingsnakes and ratsnakes. There is, however, a
strong relationship between ACSA and PCSA measurements. I could not identify a significant difference in
musculature between kingsnakes and ratsnakes that explains their different levels of constriction performance.
Unmeasured components of muscle function, such as endurance and force production, might account for
differences in performance between two species with similar muscle structure.
Key words: anatomy; cross-sectional area; Lampropeltis; muscle; Pantherophis; snake.
Introduction
For vertebrates, movement is brought about through
the use of musculature that spans the vertebral and
appendicular skeletal elements (MacIntosh et al. 2006;
Schilling, 2011). The absence of limbs in snakes relegates
all of their movements to articulations of the head, verte-
brae, ribs, and skin (Mosauer, 1935). Although the gen-
eral body plan of snakes may appear simple, it represents
an extreme degree of elongation (Mosauer, 1935; Jayne
& Riley, 2007) with immense diversity in form and func-
tion (Greene, 1997; Cundall & Greene, 2000; Lillywhite,
2014). The muscle anatomy of snakes is highly derived
and extraordinarily complex (Mosauer, 1935), so much so
that snakes have been excluded from comparative work
on the evolution of vertebrate musculature (Schilling,
2011).
Investigations into snake musculature span centuries
(Tyson, 168283; Nicodemo, 2012), but few accounts
have evaluated the anatomy of multiple muscles within
a single species (Mosauer, 1935; Gasc, 1981). Many mus-
cles span only one joint, but several muscles span multi-
ple joints with tendons of one to over 30 vertebrae in
length that connect to skeletal elements, connective tis-
sues, other muscles, and skin (Mosauer, 1935; Gasc, 1981;
Jayne, 1982). This arrangement of segmental muscles
and tendons with complex interconnections allows
sophisticated control of movements that involve few to
many joints along the body (Jayne, 1988; Moon, 2000a,
b; Young, 2010; Young & Kardong, 2010). Historically,
snake musculature was generally grouped by clade (boid,
viperid, and colubrid type anatomy; Mosauer, 1935), but
this categorization is oversimplified (Auffenberg, 1958,
1966; Gasc, 1981) and we lack anatomical descriptions
for most snake species. Snakes are an extraordinarily
diverse and important group of vertebrates (Greene,
1997; Lillywhite, 2014), yet we have a very limited
understanding of their musculoskeletal anatomy and
function. Considering the paucity of anatomical studies,
the importance of anatomy to performance (Herrel et al.
Correspondence
David A. Penning, Department of Biology & Environmental Health,
Missouri Southern State University, Joplin, MO 64804, USA.
E: davidapenning@gmail.com
Accepted for publication 31 January 2018
©2018 Anatomical Society
J. Anat. (2018) doi: 10.1111/joa.12799
Journal of Anatomy
2008), and the continued need for detailed morphologi-
cal data (Pyron, 2015), investigations describing and
especially quantifying the musculature of snakes are des-
perately needed to better understand their evolution,
function, and diversity.
Much of the recent work on muscle anatomy in snakes
has focused on the linkages between muscle cross-sectional
area and measures of performance (Lourdais et al. 2005;
Jayne & Riley, 2007; Herrel et al. 2011; Penning & Moon,
2017). Muscle cross-sectional area is used as an indicator of
muscle force production and is often measured by bisecting
specimens (or through imaging techniques on live animals)
perpendicular to the vertebral column (anatomical cross-
sectional area, ACSA). However, physiological cross-sec-
tional area (PCSA, which is the area perpendicular to the
muscle fibers) is the primary determinant of muscle force
production (MacIntosh et al. 2006) and can be very differ-
ent from ACSA. These two measures are likely to be differ-
ent because snake muscles rarely insert parallel to the
vertebral column (Mosauer, 1935; Gasc, 1981), making mea-
surements based on simple whole-body cross-sections (i.e.
ACSA) only approximations of the force-producing capacity
of the musculature (PCSA). However, to my knowledge,
there are no published measurements of PCSA of axial mus-
cles for any snake.
Here, I describe and quantify the muscle anatomy of
two colubrid snakes, kingsnakes (Lampropeltis holbrooki
Stejneger 1903) and ratsnakes (Pantherophis obsoletus
Say 1823). A notable interaction occurs between these
snakes: kingsnakes can capture, constrict, and fully ingest
larger ratsnakes (Jackson et al. 2004). Kingsnakes and rat-
snakes are both powerful constrictors, but kingsnakes can
produce significantly higher constriction pressures than
ratsnakes, despite having similar ACSAs (Penning & Moon,
2017). Whether any muscular differences underlie these
different levels of constriction performance is currently
not known. To test for any such differences, I quantify
and compare PCSAs for nine different muscles in these
species. Lastly, I compare previously reported ACSA data
(Penning & Moon, 2017) with the new PCSA data (this
study). In total, I used data from nine muscles for com-
parison. The remaining muscles were either absent or
were so small and complex that I was not able to remove
them intact.
Materials and methods
The snakes I used for anatomical investigations (L. holbrooki =7,
P. obsoletus =9) came from museum and personal collections
(Table 1). Snakes are known to exhibit longitudinal variation in
the anatomy of homologous muscles (Pregill, 1977; Nicodemo,
2012), so I analyzed the musculature at 50% snoutvent length
(SVL; Jayne, 1982). Snakes were fixed in formalin and stored in
a solution of 70% isopropyl alcohol (Simmons, 2015). Dehydra-
tion due to preservation may affect muscle mass but the relative
water loss will be the same in all muscles (Herrel et al. 2014).
Using neurosurgical tools and a stereoscopic microscope (Meiji;
3.5459magnification) illuminated with a Fisher Scientific fiber
optic rin g lamp, I isolated, measured, and removed as many
individual muscles from each specimen as possible (for a total
of nine different muscles, identified below in the results). Prior
to removal, I measured linear dimensions of each muscle with
Mitutoyo digital calipers (0.01 cm). After removal, I dried each
muscle by gentle blotting with paper towel and weighed it on
a Mettler AE 50 digital scale (to 0.0001 g). I report average val-
ues whenever I was able to remove more than one segment of
amuscle.
Measurements of muscle anatomy often include muscle mass,
muscle length, and physiological cross-sectional area (Gans & Bock,
1965; Gans & De Vries, 1987; Lieber & Friden, 2000) calculated from
the measurements described above (Alexander & Vernon, 1975;
Sacks & Roy, 1982). I calculated PCSA by dividing muscle mass by the
product of muscle density (1.06 g cm
3
from Mendez & Keys, 1960)
and muscle length (Alexander & Vernon, 1975; Sacks & Roy, 1982). I
used whole-muscle length instea d of fiber length to calculate con-
servative measures of PCSA (Herrel et al. 2014). I also measure and
report tendon lengths.
I follow the terminology of Gasc (1981) and Cundall (1982),
and use the terms insertion, anterior, and posterior to avoid
confusion when describing tendons (Moon, 2000a). In addition
to linear measures, I report muscle and tendon lengths based
on the number of vertebrae they spanned, including the verte-
brae of insertion (Jayne, 1982). In addition to these quantitative
measures, I give qualitative descriptions of muscle anatomy,
insertion sites, and interconnections where the information adds
to the previous literature. Lastly, I compare the ACSA data for
the same species from Penning & Moon (2017) to my new mea-
sures of PCSA. Penning & Moon (2017) calculated ACSA at 20%
SVL intervals. To estimate ACSA at 50% SVL, I averaged the
ACSA values from 40 and 60% SVL.
Table 1 Whole-body measurements for ratsnakes, Pantherophis
obsoletus (R), and kingsnakes, Lampropeltis holbrooki (K).
Snake
ID Sex
Mass
(g)
Diameter
(cm) SVL +TL (cm) BV +TV
R1 M 352 2.2 102.5 +20.9 237 +81
R2 M 662 2.5 131.3 +26.1 253 +86
R3 F 1047 2.9 170.6 +33.1 237 +82
R4 F 633 2.7 133.5 +29.2 240 +84
R5 M 824 2.9 153.3 +30.0 239 +80
R6 F 1274 3.3 150.9 +33.7 230 +88
R7 M 850 2.7 143.3 +30.6 232 +91
R8 F 642 2.8 141.4 +28.8 233 +91
R9 M 678 2.6 145.2 +27.5 244 +81
K1 F 634 2.6 131.5 +11.7
n
212 +33
n
K2 M 534 2.3 131.3 +16.4
n
217 +45
n
K3 F 571 2.5 116.7 +16.6 207 +49
K4 F 492 2.7 113.0 +11.3 214 +35
K5 F 506 2.8 115.5 +10.9 217 +34
K6 F 612 2.6 129.5 +14.2
n
210 +31
n
K7 F 601 2.5 126.2 +10.2
n
211 +27
n
BV, body vertebrae; SVL, snoutvent length; TL, tail length; TV,
tail vertebrae.
Superscript ‘n’ denotes nipped tail; diameter is maximum body
diameter.
©2018 Anatomical Society
Quantitative axial myology in two constricting snakes, D. A. Penning2
Statistical analysis
For quantitative comparisons, I log-transformed all data prior to
analyses. Although I used adult individuals in all of my dissec-
tions, kingsnakes were significantly smaller than the ratsnakes
(t
14
=2.43, P<0.03). To account for size variation, I incorpo-
rated size (SVL) into models where body size would affect
dependent variables. Because of the variation in two muscle
insertions (CCS and CCI, see below), and their miniscule size, I
cannot be certain that I removed all of the muscle tissue. There-
fore I report their values (Table 2) but do not include them in
quantitative analyses. To compare PCSA of all individually
measured muscles between kingsnakes and ratsnakes, while
accounting for body size, I used a repeated measures ANCOVA
(multivariate approach; Vasey & Thayer, 1987). I treat each mus-
cle as the repeated measure, species as a categorical indepen-
dent variable, and SVL as a covariate. Because serially repeated
muscle segments overlap along the body, multiple segments of
each muscle contribute to the ACSA for each muscle measured
from whole-body cross sections. Therefore, to compare the ACSA
measurements from whole-body cross-sections to equivalent
PCSA measurements, I needed to determine PCSA for the same
number of overlapping muscle segments that contributed to the
ACSA for each muscle in the whole-body cross sections. To do
this, I multiplied individual muscle PCSA by the number of seg-
ments that overlap in a single whole-body cross-section on one
side of the body and then doubled the values to create a
whole-body value. With these data, I performed the same analy-
sis as above but with this calculated whole-body PCSA as the
repeated measures variable. To compare relative muscle length
(muscle length divided by the sum of muscle and tendon
length; R uben, 19 77), I performed a repeated measure s ANOVA
with relative length of each muscle as the repeated measure
and species as the categorical variable. Because some muscles
lacked tendons (Table 2), I only include muscles in which ten-
dons were present in every specimen.
To compare the scaling of PCSA between kingsnakes and
ratsnakes, as done by Penning & Moon (2017), I summed the
whole-body PCSAs determined above for each of the four largest,
interconnected muscle groups (semispinalisspinalis complex, longis-
simus dorsi, and iliocostalis) and used a reduced-major-axis (RMA)
regression version of ANCOVA (Smith, 2009; Warton et al. 2012) with
SVL as the covariate and species as a categorical variable. I used
RMA regression to measure scaling based on the methods used in
similar studies (Herrel et al. 2011; Penning & Moon, 2017) and the
general recommendations for regression analyses based on variable
symmetry (Smith, 2009). Lastly, I quantified the relationship
between whole-body ACSA (Penning & Moon, 2017) and whole-
body PCSA for the four largest muscles using another RMA ANCOVA
with species as the categorical variable to quantify the relationship
between these two measures. I performed analyses in JMP PRO
(11.00.0) and RSTUDIO (version 0.99.441) software and consider tests
significant at P<0.05.
Results
For all 16 specimens, I was able to isolate and remove 250
individual muscle segments representing nine different
muscles (one to four segments of each muscle per snake).
Previous work has shown the incredible complexity of snake
axial musculature, and my dissections revealed even greater
complexity involving new interlinkages, muscle slips, and a
previously undescribed muscle.Below,Idescribeeach
Table 2 Gross anatomical measurements for the musculature of Pantherophis obsoletus (n=9) and Lampropeltis holbrooki (n=7).
Species Muscle ID Post tendon (cm) [V] Muscle tissue (cm) [V] Ant tendon (cm) [V] Muscle mass (g) PCSA (cm)
P. obsoletus MF 0.8 0.3 [1.52] 1.1 0.4 [23] Absent 0.033 0.011 0.028 0.009
SSP-SP 1.5 0.5 [23] 3.7 1.2 [67] 6.4 2.1 [1113] 0.054 0.018 0.014 0.005
LD Absent 3.0 1.0 [56.5] 0.8 0.3 [1] 0.051 0.017 0.016 0.005
IL 1.5 0.5 [23.5] 6.0 2.0 [1018] 1.7 0.6 [34.5] 0.060 0.020 0.010 0.003
LC Absent 1.2 0.4 [1] 0.2 0.1 [0.25] 0.050 0.017 0.039 0.013
SLS 0.4 0.3 [01] 3.7 1.2 [5.57] 0.9 0.3 [12.5] 0.027 0.009 0.007 0.002
SLI 0.4 0.1 [0.251.25] 3.6 1.2 [5.57] 0.7 0.2 [11.5] 0.026 0.009 0.007 0.002
CCS Absent 2.3 0.8 [3.54.5] Absent 0.017 0.006 0.007 0.002
CCI Absent 2.3 0.8 [34] Absent 0.013 0.004 0.005 0.002
L. holbrooki MF 1.1 0.4 [1.52] 1.2 0.4 [2] Absent 0.019 0.007 0.014 0.005
SSP-SP 1.4 0.5 [3] 2.6 0.9 [56] 4.7 1.8 [911] 0.034 0.013 0.011 0.004
LD Absent 2.1 0.8 [3.55.5] 1.3 0.5 [1] 0.042 0.016 0.013 0.005
IL 1 0.4 [13.5] 5.5 2.1 [811] 1.0 0.4 [1.252] 0.037 0.014 0.005 0.002
LC Absent 1.4 0.5 [1] 0.2 0.1 [0.25] 0.040 0.015 0.024 0.009
SLS Absent 3.9 1.5 [6.57] 0.5 0.2 [01] 0.027 0.010 0.006 0.002
SLI Absent 3.6 1.4 [67] Absent 0.019 0.007 0.005 0.002
CCS Absent 1.8 0.7 [34] Absent 0.012 0.005 0.005 0.002
CCI Absent 2.1 0.8 [34] Absent 0.009 0.003 0.004 0.001
Muscle abbreviations are as follows: CCI, costocutaneous inferior; CCS, costocutaneous superior; IL, iliocostalis; LC, levator costa; LD,
longissimus dorsi; MF, multifidus; SLI, supracostalis lateralis inferior; SLS, supracostalis lateralis superior; SSP-SP, semispinalisspinalis
complex.
Measurements are mean standard error. Note that the kingsnakes were smaller than the ratsnakes. ‘Post’ indicates posterior, ‘Ant’
indicates anterior, and values in brackets are ranges of vertebrae spanned (V).
©2018 Anatomical Society
Quantitative axial myology in two constricting snakes, D. A. Penning 3
muscle for both kingsnakes and ratsnakes. I quantify muscle
and tendon lengths as noted above and in the text wher-
ever additional details are necessary, and I provide descrip-
tive statistics (Table 2). Withtheexceptionofthelevator
costa, each muscle consists of overlapping segments that
make up longitudinal muscle columns.
Descriptions
Epaxial muscles
Each multifidus (MF) is a single triangular-shaped muscle
that inserts posteriorly on the neural spine via a short ten-
don and anteriorly onto vertebrae via two or three heads
(Fig. 1, Table 2). In kingsnakes, the MF has two anterior
heads, a medial head that inserts onto a vertebra dorsal
and posterior to the lateral head, which slopes downward
to insert onto the next anterior vertebra. In ratsnakes, the
anterior insertion of the MF is more complex, spanning up
to three vertebrae and having three distinct heads that
insert onto separate vertebrae, with the anterior-most head
being the smallest.
The semispinalisspinalis (SSPSP) complex is a two-part
muscle with multiple insertions and connections to other
muscles (Fig. 1, Table 2). The complex inserts anteriorly onto
a vertebra by a long, ribbon-like tendon; the long anterior
tendons of adjacent segments overlap and are intertwined
within thick connective tissue (Moon, 2000a) that can seem
stronger than the tendon itself. The muscle tissue spans six
to seven vertebrae in ratsnakes and five to six vertebrae in
kingsnakes; these lengths reflect muscle tissue of both the
SSPSP overall and just the SSP part, because it is longer than
the SP part. Near the anterior end of the muscle tissue, the
SSPSP complex splits into two slipsthatseparateattheir
posterior ends. The SP slip inserts dorsally on the posterior
tendon of the multifidus; the posterior tendon of the multi-
fidis spans ca. two vertebrae overall. The SSP slip continues
posteriorly onto a tendon that is continuous with the longis-
simus dorsi (Fig. 1). Data in Table 2 for the posterior tendon
of the SSPSP complex refer only to the tendon of the SSP;
there is no visible posterior tendon for the SP (Fig. 1).
The longissimus dorsi (LD) is a sheet-like muscle that con-
nects anteriorly via a forked tendon to both the SSP slip of
the SSPSP complex and the iliocostalis (IL). The posterior
insertion of the LD has two heads that insert across two ver-
tebrae onto the ventrolateral side of each vertebra (Fig. 1,
Table 2). The anterior tendon of the LD forms a sheet that
forks anteriorly, connecting dorsally with the posterior ten-
don of the SSP slip of the SSPSP complex, and ventrally
with the IL. The sheet-like tendon of the LD is an integral
part of the connective tissue partition among the three
major epaxial muscle groups (SSPSP complex, LD, and IL).
The shared anterior tendon of the LD joins the SSPSP com-
plex to the IL, forming a long musculoskeletal chain (span-
ning ca. 27 vertebrae in ratsnakes and 25 vertebrae in
kingsnakes; Fig. 1). Data in Table 2 for the anterior tendon
of the LD refer to the length of the broad, sheet-like tissue
before the tissue splits into two distinct tendons (Fig. 1).
The iliocostalis (IL) is a long, slender muscle. Each segment
of the IL muscle connects via tendons posteriorly to the LD
and anteriorly to a rib (Fig. 1, Table 2). The tendon connect-
ing the LD to the IL passes through, and contributes to, a
tough sheath of connective tissue that forms a distinct sep-
tum between the LD and IL columns in both species. From
the anterior edge of LD muscle tissue to the posterior edge
of IL muscle tissue, the ventral fork of the LD tendon spans
up to 4.5 vertebrae in ratsnakes and kingsnakes. In rat-
snakes, the IL is subdivided into an anterior and a posterior
segment of similar length, and each spans an average of
seven vertebrae (Figs 1 and 2). The intermediate tendon
between the segments is less than one vertebra in length.
As in some other colubrids, this intermediate tendon does
not have a direct connection to the ribs (Mosauer, 1935)
but is encased in connective tissue that connects the serially
repeating segments to one another. There is no intermedi-
ate tendon for the IL of kingsnakes (Fig. 1). In ratsnakes,
bothsegmentsoftheILhavetwosmallslipsoffibersthat
angle dorsally to the next anterior segment and ventrally to
the next posterior segment, braiding the adjacent segments
together and making them difficult to separate in dissec-
tion (Fig. 2). Kingsnakes show a similar but simpler pattern.
Fig. 1 Simplified schematic right lateral view
of several epaxial muscles in Pantherophis
obsoletus (top) and Lampropeltis holbrooki
(bottom). Skeletal structure is gray with
numbers representing the anterior (1) and
posterior (25 and 27) attachment sites for the
interlinked epaxial muscles. Colored areas
represent contractile tissue and white areas
represent tendons. See Table 2 for muscle
abbreviations.
©2018 Anatomical Society
Quantitative axial myology in two constricting snakes, D. A. Penning4
Ratsnakes have four total slips that come off of the IL (two
from each separate IL segment). Kingsnakes have only two
slips that come off the single IL segment.
Hypaxial muscles
The levator costa (LC) is a surprisingly large muscle (in
mass) despite its short length (Fig. 3, Table 2); it connects
a vertebra to a rib and is presumed to elevate and pro-
tract the rib. Of the muscles that I describe, this is the only
one that does not overlap along the body. This muscle
can be accessed by clipping the anterior tendons of the IL
muscle column and reflecting the entire IL muscle column
laterally (Fig. 3). The LC inserts anteriorly via a small ten-
don onto the prezygapophysial process of a vertebra and
widens posteroventrally before inserting onto the surface
of a rib approximately one-quarter of the distance from
its base to rib tip.
The supracostalis lateralis superior (SLS) and supra-
costalis lateralis inferior (SLI) muscles connect nearby ribs;
the muscle tissue runs posteroventrally and anterodor-
sally between insertions. In ratsnakes, both muscles often
have short anterior and posterior tendons (Table 2). In
kingsnakes, there were no obvious posterior tendons for
either muscle, and there was no obvious anterior tendon
on the SLI; the SLS has a short anterior tendon. Both
muscles in both species often have muscle slips that
interconnected adjacent segments. In both ratsnakes and
kingsnakes, there was a previously undescribed muscle
that separates the SLS and SLI (Fig. 4). Considering its
location between the two muscle groups, I describe it as
the supracostalis lateralis centralis (SLC). The SLC fibers
run in the opposite direction (Fig. 4), with fibers inclin-
ing anteroposteriorly. The SLC spans up to six vertebrae
with small slips inserting onto each rib along the length
of the muscle. As the SLC extends posteriorly, the seg-
ments of this muscle appear to run laterally, then dor-
sally and then medially, giving a loosely twisted or
rotated appearance. Without removal, the SLC is easily
viewed after removing the costocutaneous muscles
(Fig. 4).
The costocutaneous superior (CCS) and inferior (CCI) are
small muscles that connect the ribs to the skin, without
obvious tendons. Segments of the CCS run downward
posteriorly from ribs and attach diffusely to the skin
(Fig. 4). The CCI runs counter to the CCS; CCI segments
run slightly upward anteriorly from ribs and attach
diffusely to the skin.
Fig. 2 Right lateral view of three stretched-out iliocostalis muscle seg-
ments and their interconnecting slips in Pantherophis obsoletus (top)
and a schematic illustration of the same muscle linkages (bottom).
Each muscle is pulled ventrally so that the smaller interlinkages can be
seen.
Fig. 3 Right lateral view of the axial musculature in a ratsnake, Pan-
therophis obsoletus. The large superficial epaxial muscles
[semispinalisspinalis complex, longissimus dorsi, and iliocostalis (IL)]
have largely been removed. Portions of the IL have been cut and
reflected laterally to show the underlying individual levator costa (LC)
muscles.
A
B
Fig. 4 Right lateral view of the superficial hypaxial muscles in (A) a
ratsnake, Pantherophis obsoletus, and (B) a kingsnake, Lampropeltis
holbrooki. This view is accomplished by making a mid-dorsal incision
through the skin and reflecting it laterally, severing the costocuta-
neous muscle insertions on the skin and the fascia between the mus-
cle and skin. See Table 2 for muscle abbreviations.
©2018 Anatomical Society
Quantitative axial myology in two constricting snakes, D. A. Penning 5
Quantitative analyses
For both kingsnakes and ratsnakes, the PCSA values for indi-
vidual muscles (single-segment) range on average from
0.0038 to 0.039 cm
2
(Table 2). Of the individually measured
muscles, the LC (kingsnakes =0.024 cm
2
, ratsnakes =
0.039 cm
2
) has the highest PCSA; however, individual seg-
ments of the LC span only one vertebra and do not overlap
along the body (Fig. 3). For the single-segment PCSAs, there
is no significant interaction between muscle type and spe-
cies (repeated measures ANCOVA;F
6,7
=0.37, P>0.86). While
there is variation in PCSA across muscles (Table 2), there is
no significant difference in PCSA between species
(F
1,12
=0.05, P>0.82; Fig. 5A). In a whole-body muscle col-
umn, the total PCSA for all overlapping segments of a given
muscle visible in cross-section (on both sides of the vertebral
column) is much higher in the longer epaxial muscles. The
LD has the highest total column PCSA in kingsnakes
(0.13 cm
2
), whereas the IL has the highest total column
PCSA in ratsnakes (0.24 cm
2
). The result for total column
PCSA for each muscle is similar to the results for single-
segment PCSA. There is no significant interaction between
species and muscle type (F
6,7
=0.45, P>0.82). As with indi-
vidual PCSAs, there is variation in total column PCSA
(Fig. 5B) but there is no significant difference in total col-
umn PCSA between species (repeated measures ANCOVA
F
1,12
=0.21, P>0.65; Fig. 5B).
The relative lengths of muscle tissue and corresponding
tendons varies among muscles but not between species.
There was no significant interaction between species and
muscle identity (F
4,11
=2.37, P>0.11) and relative muscle
length was not significantly different between species
(F
1,14
=0.26, P>0.61). In general, short muscles tended to
have short tendons, and long muscles tended to have long
tendons, although there were some exceptions to these
generalizations in both epaxial and hypaxial muscles (e.g.
long posterior tendons of the MF and essentially unde-
tectable posterior tendon of the LD). Of the major intercon-
nected epaxial muscles, the SSPSP complex has the
shortest relative muscle length (ratsnakes =0.32 0.006,
kingsnakes =0.31 0.02), whereas the IL has the longest
(kingsnakes =0.80 0.01, ratsnakes =0.80 0.01).
To compare the scaling of PCSA between kingsnakes and
ratsnakes (as in Penning & Moon, 2017), I summed the
PCSAs of the four largest interconnected muscle groups
(SSPSP complex, LD, and IL) and used a reduced-major-axis
(RMA) regression version of ANCOVA (Smith, 2009; Warton
et al. 2012) with SVL as the covariate and species as a cate-
gorical variable. The summed PCSA of these four muscles
was significantly related to SVL (PCSA =3.12 9SVL 6.96,
R
2
=0.46, P<0.004; Fig. 6). However, there are no differ-
ences in the slopes (P>0.48) or intercepts (P>0.89)
between the kingsnake and ratsnake scaling patterns.
Eight snakes (four P. obsoletus and four L. holbrooki)
from my dissections (and PCSA calculations) were used in
the ACSA measurements of Penning & Moon (2017) and can
therefore be compared quantitatively to the PCSAs in this
study. The PCSA values are 5586% of the ACSA values, and
no PCSA calculation is greater than the ACSA calculation, as
would be expected for parallel-fibered muscles. The slopes
(P>0.25) and intercepts (P>0.86) are not significantly
Fig. 5 Covariate (SVL) adjusted means of log
10
physiological cross-sec-
tional area (PCSA) for individual muscles (A) and total column PCSA for
each muscle (B) at ca. 50% snoutvent length. Red triangles denote
kingsnakes (Lampropeltis holbrooki), open diamonds denote ratsnakes
(Pantherophis obsoletus). See Table 2 for muscle abbreviations.
Fig. 6 Sum of the log
10
physiological cross-sectional areas (PCSA) for
the four largest epaxial muscles (semispinalisspinalis complex, longis-
simus dorsi, and iliocostalis) at ca. 50% snoutvent length (SVL)
regressed against log
10
total SVL. Red triangles denote kingsnakes
(Lampropeltis holbrooki), open diamonds denote ratsnakes (Pan-
therophis obsoletus), and the black line represents the reduced major
axis regression model (see Results).
©2018 Anatomical Society
Quantitative axial myology in two constricting snakes, D. A. Penning6
different between kingsnakes and ratsnakes for these two
measures. The overall relationship between ACSA and PCSA
is positive (PCSA =0.95 9ACSA 0.20, R
2
=0.80, P<0.002)
and isometric based on the 95% confidence intervals (CI) of
the slope (slope CI =0.371.53; Fig. 7).
Discussion
Descriptive anatomy
In general, the epaxial muscle morphology of both rat-
snakes and kingsnakes is similar to that previously described
for other colubrid snakes (Mosauer, 1935; Gasc, 1981;
Moon, 2000a; Jayne & Riley, 2007) but with some additional
complexity. Longer muscles tended to have longer tendons
and, except for the LC, all muscles overlap along the axial
system. Ratsnakes have an intermediate tendon to the IL,
whereas kingsnakes do not. Both kingsnakes and ratsnakes
have more complex IL muscles than previously reported,
with slips interconnecting adjacent segments which gives
theILacomplexbraidedormesh-like organization. To my
knowledge, these slips have not been discussed as discrete
muscle slips in the literature (Mosauer, 1935; Auffenberg,
1958; Pregill, 1977; Gasc, 1981; Moon, 2000a; Jayne & Riley,
2007); however, interconnecting fibers have been reported
in several studies. Pregill (1977) noted that he could not sep-
arate individual IL segments from one another in Coluber
constrictor, contrasting with the results of Mosauer (1935).
Gasc (1981) did not discuss any interlinkages between adja-
cent IL segments but they appear to be partially illustrated
for Xenodon merremi (fig. 48 of Gasc, 1981) and perhaps
Hierophis viridiflavus (fig. 38 of Gasc, 1981).
I describe a new hypaxial muscle in both species that to
my knowledge has not been previously reported: the
supracostalis lateralis centralis (Fig. 4). Based on the loca-
tion, size, and insertion of this muscle, it likely aids in stiff-
eningoradductionandretractionoftheribsandinlateral
flexion of the vertebral column. For example, it may work
in concert with the SLS and SLI in locomotion (Gasc et al.
1989). The last muscle that warrants brief discussion is the
LC. Very little is said of this muscle in the literature
(Mosauer, 1935; Gasc, 1981), although it is hypothesized to
be of major functional importance in ‘snake-like’ forms
(Gasc, 1981). This muscle has the highest PCSA of any indi-
vidual muscle segment (Table 2); based on its size and loca-
tion, it likely abducts and protracts the ribs, and hence plays
an important role in locomotion, constriction, and other
feeding movements. Given the large size and likely impor-
tance of this muscle, its function should be studied in vivo
using electromyography, although instrumenting it might
be challenging because of its position underneath the LD
and IL.
Previous descriptions of snake musculature sometimes
gave conflicting results (Mosauer, 1935; Auffenberg, 1958,
1966; Pregill, 1977; Ruben, 1977; Jayne, 1982). Considering
the intraspecies variation observed in muscle and tendon
lengths (Jayne, 1982; Table 2 this study), and the lack of
standardized procedures, it is currently impossible to sepa-
rate the variation in anatomy caused by differences in dis-
section procedures from actual biological variation. In
addition to differences in simple anatomical counts and
qualitative descriptions, previous work proposes stark dif-
ferences in the hypothesized functional consequences of
anatomical complexity. Pregill (1977) stated that muscle
variation was ‘unremarkable’ with ‘minor’ differences being
additional tendons and interlacing muscles in colubrid
snakes; Gasc (1981) viewed these differences very differently
and hypothesized that differences in muscle organization
would have functional (and taxonomic) significance. Fur-
thermore, Herrel et al. (2008) showed that minor changes
in muscle angle have significant consequences for perfor-
mance between just two interconnected muscles. There-
fore, considering the incredible complexity and variation in
snake musculature, it is likely that different interconnec-
tions and linkages will reveal differences in performance
that are worth investigating and quantifying.
Quantitative comparisons
Previous work has quantified snake musculature using
anatomical cross-sectional area as an indicator of the
amount of muscle available for use (Lourdais et al. 2005;
Jayne & Riley, 2007; Herrel et al. 2011; Penning & Moon,
2017). However, it is important to measure PCSA because
it is a better indicator of the force-producing capacity of
a muscle (Sacks & Roy, 1982; MacIntosh et al. 2006) and
therefore offers a better foundation for understanding
and predicting functions. To my knowledge, no prior
quantitative data exist for PCSA in any snake, and
Fig. 7 Sum of the log
10
physiological cross-sectional areas (PCSA)
from this study regressed against log
10
anatomical cross-sectional
areas (ACSA) for the four largest epaxial muscles (semispinalisspinalis
complex, longissimus dorsi, and iliocostalis) at ca. 50% SVL from Pen-
ning & Moon (2017). Red triangles denote kingsnakes (Lampropeltis
holbrooki), open diamonds denote ratsnakes (Pantherophis obsoletus),
and the black line represents the reduced major axis regression model
(see Results).
©2018 Anatomical Society
Quantitative axial myology in two constricting snakes, D. A. Penning 7
therefore no comparisons of the actual force-producing
capacities among snakes have been made. Penning &
Moon (2017) showed that three species of kingsnakes
are capable of producing significantly higher peak con-
striction pressures on rodent prey compared with three
species of ratsnakes, despite all having similar ACSA of
the major epaxial muscles. Penning & Moon (2017)
noted that ACSA may not completely account for mus-
cle-level differences among these species. Although there
are differences in individual muscle masses, lengths, and
PCSAs in this study (Table 2), there are no differences
between P. obsoletus and L. holbrooki in the PCSA of
different muscles when compared as individual muscles
or whole cross-sections (Fig. 5). With no significant dif-
ferences in ACSA (Penning & Moon, 2017), PCSA, and
relative muscle and tendon lengths, there is currently no
identifiable anatomical mechanism that explains how
kingsnakes exert significantly higher constriction pres-
sures than ratsnakes. Similar muscle PCSA suggests that
functional differences between these species, such as
maximum force-producing abilities and feeding perfor-
mance, should be minor. However, in vivo tests of mus-
cle force and endurance could help explain the notable
difference in whole-body constriction performance. Dif-
ferences in muscle-level performance would indicate
physiological differences (muscle stress, endurance, etc.)
between these two intraguild competitors that ACSA
and PCSA are not capable of identifying. Alternatively,
similar muscle force and endurance in ratsnakes and
kingsnakes would suggest that the ability of kingsnakes
to produce higher peak constriction pressure is driven
more by behavior (coil pattern) than physiology (muscle-
level performance).
ACSA and PCSA scale isometrically and there is a
strong relationship between these two measurements
(r
2
=0.80; Fig. 7). While there is a predictable relation-
ship between these measures, it is important to note
that the regression model does not pass through the
origin (intercept 0). Therefore, ACSA overestimates
PCSA in kingsnakes and ratsnakes. Nevertheless, these
results indicate that simple ACSAs may be adequate
proxies for predicting or qualitatively comparing whole-
body performance capacity, particularly considering the
difficulty of quantifying PCSA. However, simple whole-
body ASCA is probably not a good proxy for quantita-
tive predictions or comparisons of maximum forces or
performance levels because ACSA overestimates the
force-producing architecture of a muscle (PCSA).
Acknowledgements
I thank Brad Moon for his helpful insight and guidance on snake
musculature and for providing access to several specimens. I also
thank Karen Smith for allowing access to key pieces of equip-
ment. Partial funding was provided by the Louisiana Board of
Regents Doctoral Fellowship, the Department of Biology and
Graduate Student Organization at the University of Louisiana at
Lafayette, the Louisiana Department of Wildlife and Fisheries
Rockefeller State Wildlife Scholarship, and the Kansas Herpetolog-
ical Society.
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Quantitative axial myology in two constricting snakes, D. A. Penning 9
... In the absence of limbs, the hundreds of repeating pairs of ribs in snakes are their primary skeletal structures to interact with the environment, although their functional role during locomotion is unclear. While electromyography experiments have demonstrated that the epaxial muscles produce much of the propulsive forces during most serpentine locomotor modes (Jayne 1988a;Moon and Gans 1998;Newman and Jayne 2018), our understanding of the locomotor contributions of the over fifteen serially repeated hypaxial muscles, most of which attach to the ribs, is nowhere near as complete (Mosauer 1935;Gasc 1981;Gasc et al. 1989;Moon and Gans 1998;Newman and Jayne 2018;Penning 2018;Martins et al. 2019). As organisms that locomote on their bellies, however, the locomotor forces a snake exerts must inherently be transmitted through the ribs, to the integument, and into the substrate (Cundall 1987;Capano et al. 2019aCapano et al. , 2019b. ...
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... Additionally, rib motions may (4) change body shape to contribute to the generation or maintenance of frictional reserves. Therefore, ribs may actively rotate or be stabilized to contribute to overall force production and optimization and present a wealth of opportunities for tractable hypotheses about the function of these structures during locomotor behaviors (Cundall 1987;Gasc et al. 1989;Moon and Gans 1998;Penning 2018). All of these proposed functions involve active muscular control, whereas the intrinsic morphology of the rib heads and costovertebral joints of snakes suggest a passive mechanism of equal importance. ...
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... Herrel et al. (2011) measured the CSA of five epaxial muscles (spinalis-semispinalis complex [a 2-muscle complex], multifidus, longissimus dorsi, and iliocostalis) at approximately 16.5% SVL. However, as axial musculature varies along the body in snakes (Jayne & Riley, 2007;Nicodemo, 2012;Penning, 2018;Pregill, 1975), we measured muscle CSA at five locations (20%, 40%, 60%, 80%, and 100% SVL; Penning & Moon, 2017) to assess any differences in the scaling of muscle CSA along the body. For these measurements, we took digital photographs of body cross-sections using Canon EOS Rebel T5i and Olympus Stylus Tough TG-630 cameras with scale markers in the field of view, and measured muscle CSA using ImageJ software (http://imagej.nih.gov/ij/). ...
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In many organisms, juveniles have performance capabilities that partly offset their disadvantageous sizes. Using high-speed video recordings and imaging software, we measured the scaling of head morphology, axial morphology, and defensive strike performance of Pantherophis obsoletus across their ontogeny to understand how size and morphology affect performance. Head measurements were negatively allometric whereas the cross-sectional area (CSA) of epaxial muscles displayed positive allometry. The greater relative muscle CSA of larger ratsnakes allows them to produce higher forces relative to their mass, and those forces act on a relatively smaller head mass when it is thrust forward during striking. Maximum strike accelerations of 70-273.8 ms-2 and velocities of 1.08-3.39 ms-1 scaled positively with body mass but differed from the geometric predictions. Velocity scaled with mass0.15 and acceleration scaled with mass0.17 . Larger snakes struck from greater distances (range = 4.1-26 cm), but all snakes covered the strike distances with similarly short durations (84 ± 3 ms). The negatively allometric head size, isometry of anterior mass, and positively allometric muscle CSA enable larger P. obsoletus to strike with higher velocities and accelerations than smaller individuals. Our results contrast with the scaling of strike performance in an arboreal viper, whose strike distance and velocity were independent of body mass. When strike distance is modulated, all other performance capacities are affected because of the interdependence of acceleration, velocity, duration, and distance.
... Furthermore, varanids are active foragers with high metabolic rates (Clemente et al. 2009) that use buccal pumping to overcome ventilatory-locomotor constraints (Wang et al. 1997;Owerkowicz et al. 1999), whereas green iguanas are herbivores that are constrained from simultaneous breathing and walking (Wang et al. 1997) and sustained exercise (Farmer & Hicks, 2000). Although some descriptions of the axial musculature of snakes exist (Mosauer, 1935;Pregill, 1977;Penning, 2018), comparisons between varanids and snakes are problematic due to the extreme specializations for limblessness in snakes (Gasc, 1981). ...
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Because the musculoskeletal anatomy of the trunk is the framework for the behaviors of locomotion, ventilation, and body support in lepidosaurs, comparative study of trunk anatomy in this group is critical for unraveling the selective pressures leading to extant diversity in axial form and function among vertebrates. This work uses gross dissection and computed tomography to describe the muscular and skeletal anatomy of the trunk of varanid lizards (Varanidae, Anguimorpha). Gross muscle dissections were conducted to investigate the axial muscular anatomy of Varanus exanthematicus, Varanus giganteus, Varanus rosenbergi, and Varanus panoptes. Computed tomography scans of these and additional varanid lizards from the Varanus and Odatria subgenera were conducted to investigate rib and vertebral number and gross morphology. The number of vertebrae differs between species, with 27–35 presacral and 47–137 postsacral vertebrae. Although the number of floating and abdominal ribs in varanids is variable, most species examined have three to four cervical ribs and three true ribs. Attachment and insertion points of the epaxial and hypaxial musculature are detailed. The body wall has four main hypaxial layers, from superficial to deep: oliquus externus, intercostalis externi, intercostalis internii, and transversus. Varanids differ from other investigated lepidosaurs in having supracostalis dorsus brevis (epaxial) and levator costae (hypaxial), which independently connect each rib to the vertebral column. Although more basic muscle descriptions of the body wall in reptiles are needed, comparisons with the condition in the green iguana (Iguana iguana) can be made.
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The ‘suppression’ (invalidation) for nomenclatural purposes by the International Commission on Zoological Nomenclature of the work Histoire Naturelle des Quadrupèdes Ovipares et des Serpens first published by La Cepède from 1788 to 1790 brought no benefit of any kind to zoological taxonomy and nomenclature but generated several nomenclatural problems. Here we review the history of the many discussions and proposals, as well as the successive and contradictory decisions of the Commission, regarding this work and the new nomina it contains, and we make new proposals to solve some of the problems created by these decisions. We suggest the Commission should take the initiative to restore nomenclatural availability to 18 nomina of La Cepède invalidated or of unclear status following its previous actions. More generally, we think that the use of the Plenary Power by the Commission should be more strictly regulated and made less easy and straightforward, and that the whole invalidation of complete works that have been considered as nomenclaturally available for a very long time in many works (e.g., 100 works in the 100 immediately preceding years) should be forbidden, and that the Commission should rather concentrate its attention and action on nomina rather than on works. Besides, we show that the snake nomen Coluber trigonocephalus Donndorff, 1798, currently considered valid, is invalid, and should be replaced by the nomen Coluber capitetriangulatus Bonnaterre, 1790.
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The ‘suppression’ (invalidation) for nomenclatural purposes by the International Commission on Zoological Nomenclature of the work Histoire Naturelle des Quadrupèdes Ovipares et des Serpens first published by La Cepède from 1788 to 1790 brought no benefit of any kind to zoological taxonomy and nomenclature but generated several nomenclatural problems. Here we review the history of the many discussions and proposals, as well as the successive and contradictory decisions of the Commission, regarding this work and the new nomina it contains, and we make new proposals to solve some of the problems created by these decisions. We suggest the Commission should take the initiative to restore nomenclatural availability to 18 nomina of La Cepède invalidated or of unclear status following its previous actions. More generally, we think that the use of the Plenary Power by the Commission should be more strictly regulated and made less easy and straightforward, and that the whole invalidation of complete works that have been considered as nomenclaturally available for a very long time in many works (e.g., 100 works in the 100 immediately preceding years) should be forbidden, and that the Commission should rather concentrate its attention and action on nomina rather than on works. Besides, we show that the snake nomen Coluber trigonocephalus Donndorff, 1798, currently considered valid, is invalid, and should be replaced by the nomen Coluber capitetriangulatus Bonnaterre, 1790.
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Across ecosystems and trophic levels, predators are usually larger than their prey, and when trophic morphology converges, predators typically avoid predation on intraguild competitors unless the prey is notably smaller in size. However, a currently unexplained exception occurs in kingsnakes in the genus Lampropeltis. Kingsnakes are able to capture, constrict and consume other snakes that are not only larger than themselves but that are also powerful constrictors (such as ratsnakes in the genus Pantherophis). Their mechanisms of success as intraguild predators on other constrictors remain unknown. To begin addressing these mechanisms, we studied the scaling of muscle cross-sectional area, pulling force and constriction pressure across the ontogeny of six species of snakes (Lampropeltis californiae, L. getula, L. holbrooki, Pantherophis alleghaniensis, P. guttatus and P. obsoletus). Muscle cross-sectional area is an indicator of potential force production, pulling force is an indicator of escape performance, and constriction pressure is a measure of prey-handling performance. Muscle cross-sectional area scaled similarly for all snakes, and there was no significant difference in maximumpulling force among species. However, kingsnakes exerted significantly higher pressures on their prey than ratsnakes. The similar escape performance among species indicates that kingsnakes win in predatory encounters because of their superior constriction performance, not because ratsnakes have inferior escape performance. The superior constriction performance by kingsnakes results from their consistent and distinctive coil posture and perhaps from additional aspects of muscle structure and function that need to be tested in future research.
Chapter
Body elongation and limblessness have evolved significantly within Tetrapoda, typically associated with aquatic, fossorial, crevice dwelling, or grass-swimming lifestyles. Some lineages of secondarily elongate vertebrates (for example, limbless skinks) have solved the concomitant problem of reduction in size of the feeding apparatus by eating many tiny items, whereas others (for example, some caecilians) shear ingestible chunks out of large prey. Many advanced snakes achieved a third solution by radically restructuring their heads and feeding infrequently on large items; perhaps not coincidentally. Among limbless squamate reptiles, only Serpentes has achieved substantial adaptive radiation and high species richness. More than 2,500 species of living snakes inhabit most temperate and tropical land masses, and they often are prominent predators in terrestrial, arboreal, fossorial, aquatic, and even marine faunas. Snakes eat prey as different as onycophorans, fish eggs, centipedes, cormorants, and porcupines; many species commonly consume individual items weighing 20% of their own mass, and some venomous species occasionally subdue and eat prey that exceed their own mass by as much as 50%. This chapter first briefly surveys snake diversity and then examines in detail the functional and morphological aspects of capturing, swallowing, and processing prey that generally characterize relatively derived subgroups. It only touches on sensory aspects of feeding.
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The time is past when a research program in systematics should be based on only a few genes, extant taxa, and ultrametric trees. Cheap genome sequencing, powerful statistical methods, and new fossil discoveries promise to reinvigorate research programs in evolutionary biology. Population genetics, phylogeography, and species delimitation all benefit from genomic data, not just tree building alone. Null-hypothesis testing and power analysis via simulation can increase the confidence and robustness of phylogenetic comparative methods. Merging morphological and molecular datasets for fossil and extant taxa gives a more complete view of the Tree of Life. Combined, these developments can foster a post-molecular systematics, integrating phylogenetic signal from the population up based on DNA and through time based on direct observation rather than inference. Copyright © 2015 Elsevier Ltd. All rights reserved.