This article isThis article protec 10.1111/jeb.13251 doi: differences to lead between the of thisversion citethisarticle and asVersion Record.Please copyediting, paginationbeen throughthe andproofreadingtypesetting, process,may which This article acceptedhas been for publication andundergone full * corresponding 7RX,UK Hull, HullHU6 of University 2 Germany 1 Blanke Alexander head strain. to strain of mapping ridge many toone a for Evidence capsules: head insect orthognathous and prognathous of analysis biomechanical A Title page Papers :Research Article type 0000 ID: (Orcid BLANKE DR ALEXANDER A biomechanical analysis of progn analysis A biomechanical Medical and Biological Engineering Research Group, School of Engineering of School Group, Research Engineering Biological and Medical Accepted Cologne, 50674 47b, Straße Zülpicher Cologne, of University Biocenter, Institute, Zoological Article
author 1,2 * , Manuel Manuel Pinheiro ted byted copyright. All rights reserved.
many to one mapping of mapping many toone
athous and orthognathous insect orthognathous athous and
2 , Peter J. Watson Peter - 0003 - 4385 ridge ridge -
6039) strain to strain 2 , Michael Michael
head strain J. Fagan
head capsules head peer peer review buthasnot 2
.
and Computer Computer and : Evidence for a for : Evidence Science, Science, This article isThis article by protected copyright. All rightsreserved. and species, epistomal, all genal/subgenal, in the loaded highly as consistently such are structures areas peculiar circumoccular of range a that show We influence the compare and quantify to order in analysis element finite and modelling dynamics multibody w these assess we Here, head. the to endoskeleton the of connection the and size eye orientation, mouthpart general the are changes anatomical prominent most the of some stoneflies, unclear are performance variable remarkably are shapes head Insect Abstract codes eCSE04 Service, project programme CSE embedded the and EP/1006753/1, “Mech 1355/1 BL (DFG: Forschungsgemeinschaft Deutsche the by supported was AB acknowledged. Elektronen gratefully is experiments synchrotron Deutsches the of support financial The Funding version. Forfic of model MDA the of model MDA the except tests and analyses all conducted AB study. the designed and conceived MJF and AB Contributions Author Cologne, 50674 47b, Straße 466664 1482 Zülpicher Cologne, of Germany University Biocenter, Institute, Zoological Blanke Alexander author Corresponding
Accepted as ell Article -
Evo
differing ridge and sclerite configurations configurations sclerite and ridge differing
;
of anatomical changes anatomical of the earwig the e - Insect”) - mail
address
Dvlpet f VOX of Development . . MSP helped to generate histograms of the strain distribution and PJW set up up set PJW and distribution strain the of histograms generate to helped MSP .
contact information contact . Among . ula. All authors contributed to manuscript to contributed authors All ula. : a.blanke@ - 11 andeCSE01
on on “ basal strain in particular head regions and the whole head andthe whole head regions particular in strain uni ” -
koeln.de winged insects, such as dragonflies, mayflies, earwigs, and earwigs, mayflies, dragonflies, as such insects, winged - : FE2 was supported by EPSRC grants EP/1006745/1 and and EP/1006745/1 grants EPSRC by supported was FE2
- but the influences of these changes on biomechanical biomechanical on changes these of influences the but 15.
;
T l (n) +49 (Uni): el. using - of the ARCHER UK National Supercomputing Supercomputing National UK ARCHER the of ycrto (EY I (DESY: Synchrotron - 1)
and by an ERC starting grant (ID: 754290 754290 (ID: grant starting ERC an by and modern engineering methods methods engineering modern
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writing 221 despite drastically drastically despite
4 - a research fellowship of of fellowship research a
70 20120065) to perform perform to 20120065) and approved the final final the approved and
76128 ; . variations a: +4 Fax:
including differing 9
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This article isThis article by protected copyright. All rightsreserved. mapping one challenges adaptive same the meet complex I Introduction analysis, insect, Keywords head loading of mapping one to many context, evolutionary an coul which orientation mouthpart configuration endoskeleton the of irrespective capsule appears eyes the as such structures vulnerable and capsule area epistomal the and endoskeleton region head mouthparts. projecting downward with capsule head the to arms endoskeletal dorsal the strain capsule head on influence (orthognathous) morph Accepted s single systems functional complex n Article ologies in species species in ologies
dnt, peeotr, Polyneoptera Ephemeroptera, Odonata, ht b that endoskeleton, mandible, orthognathous, prognathous orthognathous, mandible, endoskeleton, is maintained is
reveals that reveals indeed (MTOM) iting mouthparts. mouthparts. - chewing could have fostered fostered have could of form to the same function same the to form of in an optimal way. Multiple morphological combinations combinations morphological Multiple way. optimal an in c oncerted changes in changes oncerted general general ih owr projecting forward with
od ae aae by managed are loads allow estvt aaye so ta the that show analyses Sensitivity
d be an explanation for the variability of this trait among insects. among trait this the variabilityof for explanation be an d if a circumoccular ridge is present. In contrast, the connection of of connection the contrast, In present. is ridge circumoccular a if mouthpart mouthpart
or react in multiple ways to changing conditions changing to ways multiple in react or for for lead to a consistent relative loading loading relative consistent a to lead tructures the dynamic dynamic the more nlss f h rltv strain relative the of Analysis and head orientation head and
radical edsbtutrs uha h ugnlae, th area, subgenal the as such substructures head ,
could especially affects overall head loading in species species in loading head overall affects especially al performance al
finite element analysis, analysis, element finite strain patterns onto a relatively similar overall overall similar relatively a onto patterns strain system a n rgahu ad rhgahu insects. orthognathous and prognathous in
diversification diversification
(prognathous) anatomical changes such as as such changes anatomical
evolve evolve
of strengthening ridges on the head head the on ridges strengthening of hl the while presence of of presence
. (Arnold, 1983) (Arnold, processes seen processes C
oncerted changes in ridge and and ridge in changes oncerted and downwards projecting projecting downwards and bten pce f species between s
overall function of the the of function overall eyes multibody dynamics dynamics multibody o the for could
is thought to thought is in insects. in has . This many to many This .
be suitable to to suitable be
the whole head head whole a negligible negligible a or each each or general
lead lead
In In It It e
This article isThis article by protected copyright. All rightsreserved. D connection) ( herbivorous are mainly mayflies and connection) DTA (cuticular predators are dragonflies o are DTA) soft a (with stoneflies and DTA) stiff a prefere food that unlikely cutic stoneflies difference. general endoskeleton the (forwa prognathous as well as orthognathous 2014) axis the to respect with downwards oriented are mouthparts the mayflies and dragonflies size eye and capsule, head the to endoskeleton the and stoneflies mayflies, Three I to be difficult might spaces performance and sources, food similar despite systems feeding where instances many are there al. et space performance mechanical similar a onto map but lengths different have elements bony four the where fish, of apparatus feeding the of linkage bar four the is MTOM m if overestimated be diversification to nsects ragonflies show large protruding and dome shaped eyes (with stiff DTAs), mayfly eyes are smaller smaller are eyes mayfly DTAs), stiff (with eyes shaped dome and protruding large show ragonflies Accepted Article a (orthognathous) le , 2008; Cooper & Westneat, 2009; Martinez & Sparks, 2017; Thompson Thompson 2017; Sparks, & Martinez 2009; Westneat, & Cooper 2008; ,
distinct
osdrbe degr considerable are a prime example for for prime example a are otiig iegs uh s rshpes eris trie ad cockroaches and termites earwigs, grasshoppers, as such lineages containing in in
all studied studied all Cihl, 92 Muis 16; tnce, 200 Staniczek, 1968; Moulins, 1962; (Chisholm, .
Additionally, the size of the eyes the of size the Additionally,
changes among among changes (Wainwright (Wainwright
o h head the to nta, t Instead, ,
while while dragonflies and earwigs earwigs and dragonflies orphological evolution evolution orphological earwigs, are the general orientation of the mouthparts, the connection of of connection the mouthparts, the of orientation general the are earwigs, nce or phylogeny are the are phylogeny or nce ee the et al. et
e Ts r cnetd by connected are DTAs he of of the earliest divergences of divergences earliest the
so by such such , 2004, 2005) 2004, , -
morphological diversity diversity morphological called Polyneoptera, called the dorsal tentorial arms (DTAs) arms tentorial dorsal the extreme extreme
thus thus detect. the ways of morphological morphological of ways the
varies varies differences differences . s ucinly neutral functionally is d rjcig mouthparts projecting) rd
(Kadam, 1961; Blanke Blanke 1961; (Kadam, Also, the significance of morphological change could could change morphological of significance the Also,
show show mnivorous causes of this variation, since both, earwigs (with (with earwigs both, since variation, this of causes significantly
more (
probably probably Sogas 13; Beutel 1935; (Snodgrass,
in the morphology of food uptake system uptake food of morphology the in biting
soft soft 0) u mgt al might but fundamental
( , whereas whereas , Popham, 1959; Bo Bo 1959; Popham, -
ligament chewing insects such as dragonflies, dragonflies, as such insects chewing with a monophyletic monophyletic however, , in the four mentioned lineages: mentioned four the in . A widely studied example of of example studied widely A t al. et
u tissue ous (Alfaro (Alfaro t is it .
morphological differences morphological T so decrease functional functional decrease so piiain o similar to optimization e osl connection dorsal he 21, 2013) 2012, , et al. et composed composed
do et al. et taxon et al. et es , 2017) ,
t al. et
n afis and mayflies in not reflect this this reflect not , 2004; Parnell Parnell 2004; , cephalocauda , 2007) , (Misof (Misof 2014) , . sclerotized sclerotized .
H It seems seems It s owever, owever, oft DTA DTA oft )
etal. while while have . In In . of of s , . l
This article isThis article by protected copyright. All rightsreserved. analysi element finite using investigated are study shape. in changes multidimensional and changes size isometric of irrespective specimens different in structures equivalent of behaviour mechanical the of comparison a for allow str relative specimen, given a on visible metrics shape obvious more immediately to not compared accessible is metric a such Although specimen. same the in structure another to relative per biomechanical define we context, this In head. whole the even or head the of regions certain in performance biomechanical pro with associated uptake. food during capsule head the of loading overall on structures these of influence the understand to investigated are connection endoskeletal this In are possible. uptake food regions head of morphology the influence also input sensory of requirements functional its to adapted is system uptake food each theory, Beutel morphological dependent lineage the describe to straightforward is it While bite forces influence on endoskeleton the to attached adductors associated smaller lineage a and head the of backside the to attached adductor mandibular two with attached are They construction. principal same the of mandibles show lineages four the variety, l two other the while DTAs), soft have (but capsule head the of outline overall the in integrated and Accepted Article capsule. head the of rest the to compared eyes smaller even have ineages ball context, the study has two aims. Firstly, the aforementioned differences in eye size and dorsal dorsal and size eye in differences aforementioned the Firstly, aims. two has study the context, et al. et - and , 2014) , - socket , the biomechanical consequences of such morphological changes are unclear. unclear. are changes morphological such of consequences biomechanical the , -
joints, joints, and orthognathy are investigated to determine whether they lead to a similar similar a to lead they whether determine to investigated are orthognathy and (David (David
one anterior and one posterior to posterior one and anterior one formance as the strain (or deformation) occurring in a given structure structure given a in occurring deformation) (or strain the as formance et al.
hrceitc o ponty n orthognathy and prognathy of characteristics , 2016b;a) ,
(mainly eyes and antennae) and eyes (mainly above mentioned mentioned above .
so that only suboptimal suboptimal only that so s (FEA), an engineering technique which technique engineering an (FEA), s
eody th Secondly, environment environment
the head, and moved moved and head, the Fgr 1 (Figure opooia changes morphological e suite of morphological changes changes morphological of suite e but
and even flight styles might styles flight even and
biomechanical biomechanical ) te fcos uh s the as such factors other
- which have a negligible negligible a have which dependent set of 1 to 4 to 1 of set dependent y otat o this to contrast By
oh is f this of aims Both Sogas 1935; (Snodgrass, primarily primarily solutions for for solutions and derive derive and
provides provides by a by ains ains In In
This article isThis article by protected copyright. All rightsreserved. coordinates. al. ITK software source open the with performed was stacks image reconstructed Deutsche the of P05 then water remove to BioRad) E4850, (Model point critical 1989) (Romeis, from obtained stage larval the during realised uptake food the of most stage adult the in habits feeding and preference food in changes show stoneflies while mating to adapted shapes head specialised highly and mouthparts vestigial f evolution, earwig the auricularia lacustris used We methods and Materials species. between strains theseof relative a by followed head whole the or regions, head other to relative region head each in strain the of analysis an by investigated is performance biomechanical the while FEA, during head is the strain capsule on connection endoskeletal dorsal the and eyes of influence The uptake. food during corresponding the and head, the across deformations the about information
Accepted2006 , Article scanned using synchrotron micro synchrotron using scanned
)
(Ephemeroptera: Siphlonuridae), Siphlonuridae), (Ephemeroptera: to obtain high resolution 3D models of the head capsules and muscle origin and insertion insertion and origin muscle and capsules head the of models 3D resolution high obtain to
single specimens from from specimens single . (Dermaptera: Forficulidae). Forficulidae). (Dermaptera:
inal instar larvae larvae instar inal Although aquatic larval stages are considered a secondary development during insect insect during development secondary a considered are stages larval aquatic Although
and washed with in ascending order ascending in with washed and loo peevd aua hsoy collections history natural preserved alcohol assessed by systematically altering the material parameters of these structures structures these of parameters material the altering systematically by assessed s Elektronen Synchrotron (DESY DORIS III and PETRA III). Segmentation of the the of Segmentation III). PETRA and III DORIS (DESY Synchrotron Elektronen s
a t be to had or species four - computed tomography (SRµCT) at the beamlines BW2 and IBL IBL and BW2 beamlines the at (SRµCT) tomography computed A
dult specimens were used in the case of the dragonfly and and dragonfly the of case the in used were specimens dult
sd o te te two other the for used Perla Lse virens Lestes , marginata
with 70 with without - . 100% EthOH before drying them at the the at them drying before EthOH 100%
, fixed with alcoholic Bouin’s solution solution Bouin’s alcoholic with fixed ,
Specimens were collected locally or or locally collected were Specimens heavy heavy (Plecoptera: Perlidae) and and Perlidae) (Plecoptera:
(Odonata: Zygoptera), Zygoptera), (Odonata:
species organ shrinkage organ (Rúa & Figueroa, 2013) Figueroa, & (Rúa ic adult since
subsequent comparison comparison subsequent
- stresses and strains, strains, and stresses snap snap . (Yushkevich (Yushkevich mayflies have have mayflies S amples were were amples Siphlonurus Siphlonurus Forficula Forficula seem to to seem
with with et et This article isThis article by protected copyright. All rightsreserved. conditions. Accepted2012) Segmented setup. MDA about the details S1 for loading mouthpart during capsule head the on occurring i model, element finite mandibles force bite forces, which (MDA), analysis dynamics multibody using specimen each in arrangements muscle the modelled we Therefore, results. meaningful produce metric) based corresponding the and head, the across deformations the about information obtain to (FEA) analysis element finite used we Second, biting. during muscle forces divi by FTC) coefficient, transmission (force item Article food the to forces muscular of transmission the of effectiveness the calculated we Furthermore, angles axis joint as to referred (henceforth axis rotation joint the to reference a as insertion attachment muscle the of centroid the between axis the taking by 1b) Fig. axis”, (“rotation joints mandible spherical two the between spanning axis virtual the to relative ( BLENDER software source open the in models surface 3D segmented the on measured were ratios surface alone. levels. two at studied for measures biomechanical were systems head four the of biomechanics The Analysis Biomechanical
with the the with The mandibular mechanical advantage (MA = in = (MA advantage mechanical mandibular The www.blender.org uig od uptake food during 3D models 3D T peet re oy motion body free prevent o . FEA requires information about the physiological forces acting on the system to to system the on acting forces physiological the about information requires FEA . predicted (BF) (BF)
were imported into the open the into imported were n order to obtain information about the patterns and magnitudes of strain strain of magnitudes and patterns the about information obtain to order n
n jit ecin forces reaction joint and bite force, JRFs and JRFs force, bite
). the
The insertion angle of the main mandibular adductor was measured measured was adductor mandibular main the of angle insertion The . These physiologically representative forces are then applied applied then are forces representative physiologically These . mandible food uptake system which can be obtained from obtained be can which system uptake food mandible
tess n sris uig od uptake food during strains and stresses
due to rounding errors in the solution phase, phase, solution the in errors rounding to due individual individual ding the total total the ding
allo (JRFs)
source finite element solver VOX solver element finite source - ws ws lever to out to lever . muscle strand forces applied as the as applied forces strand muscle
Please refer to the supplementary material material supplementary the to refer Please ) that must be acting on the head and and head the on acting be must that ) for for
n estimat an estimated bite force by the sum of of sum the by force bite estimated - lever ratio lever
ion ra n te mandi the and area
ie a (i.e.
of the forces (muscle (muscle forces the of ) and the eye the and ) First, we obtained obtained we First,
force - FE2
plus plus (Liu (Liu - to loading
, JAA , shape shape shape shape - et al. et three three bular bular head head to
). a ,
This article isThis article by protected copyright. All rightsreserved. Paraview software were example, for strain the how investigate Blanke 2001; 2000, (Staniczek, Mat 1963; Kéler, biting the for relevant being as previously hypothesized were head. complete the and eye, the head the connection, DTA eye, (G/SG), ridge/area (sub)genal (ER), ridge/area epistomal corpotentorium (DTA), arms tentorial dorsal (ATA), arms tentorial (most minimum and tensile) (most maximum str principal the compressive) extracted then we results FEA the From the of gives anoverview (350MPa; tissue ligamentous “soft” for literature the stiffness different with simulated also were (DTAs) arms tentorial dorsal and deformation. negligible experience should eyes that expected we and lineages on effect The properties. material different using by results the confound to wish not did and levels strain relative and patterns strain on shape of influence the in only interested are we since species, three other the with dragonfly) al. materials all for assumed was 0.3 of ratio Poisson’s Blanke 2011; Schmitz, & Klocke 1992; Pharr, & (Oliver dragonfly the for measured ( direction all in constrained also were foramen occipital the at nodes separate Young’s Young’s
Accepted Article Nikolov 2009; , strain patterns was investigated (in all species), since DTA since species), all (in investigated was patterns strain thus thus moduli repeatedly repeatedly
h woe ed r h ee alone. eyes the or head whole the )
ua 1965) suda, of parts of et al. et
(Ahrens (Ahrens , 2010) , eetd sn cso srpig n h visualisation the in scripting custom using selected material parameter combinations parameter material s of of is ( ains
et al. et in by arms) tentorial anterior and (clypeus capsule head the
. the tentorial and ridge/sclerite areas areas ridge/sclerite and tentorial the especially in considerations considerations in especially We used the same material parameters (obtained for the head o head the for (obtained parameters material same the used We et al. et
of of ɛ nano , 2005) , 1
changing mate changing The tentorium and ridge/sclerite area ridge/sclerite and tentorium The and , 2017b) , - indentation indentation
to ensure that the same elements were selected after each each after selected were elements same the that ensure to ɛ 3
respectively) for the following head regions: regions: head following the for respectively) .
The rest of the head and eye regions were chosen chosen were regions eye and head the of rest The rial properties of of properties rial
The respective elements within each FEA model model FEA each within elements respective The ne wt conditions wet under
based on studies of lobster cuticle lobster of studies on based (Zajac, 1989; Maganar 1989; (Zajac, t al. et
used for each foreach used of -
chewing - the evolution of stronger bite forces forces bite stronger of evolution the head connections are variable across across variable are connections head 2017a) , the eyes and tentorial structures structures tentorial and eyes the relate
(CT)
process process
Splmnay et S1). text (Supplementary FEA FEA s tentorium whole ,
using established routines routines established using to the strain occurring on occurring strain the to
were chosen were is model
values suggested from from suggested values
(Snodgrass, 1935; von von 1935; (Snodgrass, s. s. et al. et n post and
Therefore, Therefore, Material properties properties Material . , 1998) ,
and eyes were were eyes and (Fabritius (Fabritius since the since - processing excluding excluding ). Table 1 Table ). the eyes eyes the Anterior Anterior
(TENT) f the f
se to to et et A , ,
This article isThis article by protected copyright. All rightsreserved. 67 of angle an at inserts adductor mandibular 2 Table (“JAA”, angles axis example, for with, variable were Siphlonurus MAs the however, respectively, 0.50 and 0.53 of mandibles biting. during joint posterior the at in have an of ratio The whereas = FTC coefficient, adductor. main 90% species, other the in whereas production, force muscle lo comparatively a makes adductor main stone mayfly The muscle morphology, General Re in this resulted regions. head other the to relative region each of loading relative the independ size a obtain to pairs region head of combination possible every of IQRs of 3 (IQR; distributions strain species between strain compare simulation Perla Accepted Articlesults nearly equal force distribution between the anterior and posterior mandibular joints whereas whereas joints mandibular posterior and anterior the between distribution force equal nearly fly
and and Perla Siphlonurus . To study how the chosen head regions compare in their strain to each other and to to and other each to strain their in compare regions head chosen the how study To
Siphlonurus retu Forficula
had the highest (0.816 highest the had 90
eir o post to terior rning a similar MA MA similar a rning The most effective transmission of muscle force force muscle of transmission effective most The
total BF/sum of left and right muscle forces muscle right and left of BF/sum total
co
mbinations of head region pairs ( region pairs head of mbinations was
the anterior mandibular joi mandibular anterior the
showed the lowest lowest the showed
the least effective the least rd rltv t te uce neto soe ta in that showed insertion muscle the to relative )
minus 1 minus - ro JF (JF ai” Tbe 2 Table ratio”, (“JRF JRFs erior
and bite forces bite and ,
we calculated the respective interquartile range of the principal principal the of range interquartile respective the calculated we of 0.52 for the right mandible, but only 0.42 for the left. the for 0.42 only but mandible, right the for 0.52 of st N). The predicted muscle forces showed that in that showed forces muscle predicted The N).
Forficula quartile of a given distribution). We then calculated the ratio ratio the calculated then We distribution). given a of quartile w contribution (~61 contribution w (~22%). predicted predicted
also also - 3 rltv t te joi the to relative 73° nt is only loaded with 32 with loaded only is nt
showed the highest MA for the left and right right and left the for MA highest the showed 45 bite force ( force bite
each for each
or more or revealed ) )
- 67%, Table 3 Table 67%, was shown by shown was ɛ BF, BF, 1 to bite force force bite to and
of the force is generated by t by generated is force the of 0.067N, Table 2) whereas the the whereas 2) Table 0.067N, nt axis, whereas in all other other all in whereas axis, nt
With
that that ɛ 3 - ). ) of the overall mandible mandible overall the of ) 64% of the force present present force the of 64%
ten Forficula Siphlonurus Siphlonurus
single head regions head single (force transmission transmission (force Siphlonurus ent measure of of measure ent
( 39
%, Table 2 Table %, and and
the main main the The j The Lestes oint oint
the the he he )
This article isThis article by protected copyright. All rightsreserved. relative corpotentorium arms a dragonfly the in R whole tentorium regions arms IQRs most (6.58) dragonfly the in head complete the and DTA the between ratio (0.05) dragonfly the in DTA the and eye the between ratio the (6.41), dragonfly the and (0.07) the are cases extreme Exemplary each for IQRs Relative regions. these strainin higher showed although species two other as 2) such SR, Fig. (ER & well a with species those In 2). Fig. arms, tentorial anterior the at (especially endoskeleton the and antennae the of base the area, subgenal the joints, posterior ( strains principal minimum and maximum high showed species All biting Strain during in value thehighest with magnitude of insertio the species Accepted IQRs elative Article ,
the n te psoa ridge epistomal the and
whereas the spread was lower when lower was spread the whereas Siphlonu genal/subgenal area (or ridge) and the DTAs the and ridge) (or area genal/subgenal for each head r head each for of highly loaded areas such as such loadedareas highly of
to single head regions to single comparatively rus n angle is close to 90° (Table 2 (Table 90° to close is angle n
the
with its slightly thickened and bended subgenal and epistomal areas, also also areas, epistomal and subgenal bended and thickened slightly its with head region pair showed showed pair region head Lestes strain was more evenly distributed in the subgenal and epistomal area, area, epistomal and subgenal the in distributed evenly more was strain
to the dorsal tentorial arms arms tentorial dorsal the to egion pair showed a comparatively wide distribution wide comparatively a showed pair egion
and
higher proportion of strain is strain of proportion higher Fg 4). (Fig.
Forficula strain ratios ratios strain
Lestes
(Fig. In the stonefly, stonefly, the In , ridges and endoskeletal endoskeletal ridges and 3). 3). the
comparing the eye the comparing (0.71) and the lowest in andthe lowest (0.71)
a wide distribution of strain ratios between species. species. between ratios strain of distribution wide a strain was also high in these regions, regions, highthese in also was strain between the dorsal dorsal the between ). The eye The
were n te et f h tentorium the of rest the and - - developed epistomal and subgenal ridge ridge subgenal and epistomal developed to
more highly loaded than all other head head other all than loaded highly more
t accommodated he anterior tentorial arms arms tentorial anterior he - head surface ratio varied by an order order an by varied ratio surface head , the complete head cap head complete the elements Forficula tentorial arms in the stonefly stonefly the in arms tentorial ɛ & 1
(Fig. 3, Table S1) Table 3, (Fig. ɛ
3) at the anterior and and anterior the at 3)
showed ,
by the dorsal dorsal the by
(0.08). the anterior tentorial tentorial anterior the
whereas in the in the whereas that sule showed the the showed .
especially especially Although tentorial n the and
and the the and , or the the or ,
This article isThis article by protected copyright. All rightsreserved. Accepted forces bite larger from resulting the in changes morphological Davi setups mandibular and widths head comparable forces. with insects other for bite measurements force bite earlier with line in are study present the in predicted larger show really volumes) muscle thus (and sizes head 2016b) forces bite insect broad and ridges epistomal Neoptera two the and dragonfly the mayfly, the to Compared forces bite higher of development Neoptera and Odonata in arms tentorial anterior ball mandibular observations morphological earlier on Based ArticleDiscussion in distribution strain Siphlonurus in changes higher to lead arms tentorial dorsal the of properties material in capsule head the of distribution strain on influence (<1%) insignificant an have eye the of changes property material different for arms tentorial dorsal and eyes, head, the in frequencies strain relative cumulative the of Histograms ridge to the epistomal relative tentorial arms highest d et al. et
it was however unclear whether insect whether unclear however was it strain
, 2016b) , Lestes
(~8%) and (~8%) and
whereas the earwig the whereas - and , (Wheater & (Wheater Forficula . Given the increase in bite force from mayflies from force bite in increase the Given . - socket joints, a strong genal/subgenal area (with a subgenal subgenal a (with area genal/subgenal strong a joints, socket Lestes obntos ( combinations
anterior anterior
and and (~5%) compared to compared (~5%)
Evans, 1989; Goyens 1989; Evans, bv mnind tutrs loe to allowed structures mentioned above Perla and the mayfly the and .
u boehncl study biomechanical Our oprd o afis n silverfish and mayflies to compared tentorial arms. arms. tentorial Supplementary Supplementary
whereas the effect was >20% in in >20% was effect the whereas , it has been has it , /area and the rest of the ofthe tentorium therest and /area s
Perla from these different lineages but with comparable comparable with but lineages different these from
showed a co a showed (Wheater & Evans, 1989; Weihmann 1989; Evans, & (Wheater et al. et Due to the s the to Due ,
Fig. and and probably played an important role in the the in role important an played probably , 2014; Weihmann Weihmann 2014; , hypothesised hypothesised Forficula Forficula S1
) showed that the simulated material material simulated the that showed ) mparatively high strain high mparatively have basically basically parse literature record concerning concerning record literature parse
to Neoptera, Neoptera, to (~1%).
eldvlpdsbea and subgenal developed well that the evolution of anterior anterior of evolution the that better
ofrs th confirms Siphlonurus Saizk 20, 2001) 2000, (Staniczek, ned t Indeed, et al. et . distribute
this implies that implies this , 2015; David 2015; , ridge) and strong strong and ridge)
e bite he in the anterior anterior the in . ese et al. et Variation in in Variation
the strain strain the previous previous
, 2015; 2015; , forces forces et al. et the the , . This article isThis article by protected copyright. All rightsreserved. structures of role mechanical the assess to used were comparisons closely phylogenetically 2017) Sparks, & Martinez 2016; Butler, & Scales al. wider a shap with transmissions force over correlate and sample specimen transmissions force estimate to calculations lever of types different with analysis FEA using assessed to ratios strain different eye the and capsule head the of rest the in strain similar overall an mentioned tran of proportion the in changes concerted that suggests species four all or three least at across similar are which ratios strain show capsule head and prognathy (Fig. specific species still is other each to compared structures reinforcement as endoskeleton anterior Despite and broad S1). from obvious immediately ridge mayfly the 2001) 2000, (Staniczek, biting during similar largely arms tentorial dorsal and anterior area epistomal and genal/subgena the as such structures of range biomechanical
Accepted Stoessel 2009; , Article
Apparently, positive selection for a strengthening of the front the of strengthening a for selection positive Apparently, is rather rather the general similarities in strain patterns strain in similarities general the ened
in the same same the in reinforcement structures (or their precursors their (or structures reinforcement weakly developed developed weakly suggestions
orthognathy or the role of the DTA connection. DTA the of role the or orthognathy tentorial arms arms tentorial et al. et (Pierce (Pierce , our data our , - areas where epistomal and subgenal ridges can be expected (the expected be can ridges subgenal and epistomal where areas
, 2013; Anderson Anderson 2013; , related species which species related a largely similar relative strain of the whole head capsule head whole the of strain relative similar largely a : et al. et
visual inspection of the of inspection visual between the four species four the between A lthough the head morphologies considered here are here considered morphologies head the lthough allowed allowed , 2008; Stayton, 2011) Stayton, 2008; ,
and shows that shows ,
a a e ossety ne hg load high under consistently re higher bite forces in Odonata and Neoptera. and inOdonata biteforces higher
subgenal ridge subgenal et al. et the aforementioned strain patterns strain aforementioned the show variation in a functional subsystem. subsystem. functional a in variation show , 2014; Collar Collar 2014; ,
and the mechanical importance of ridges and the and ridges of importance mechanical the and Common . strain patterns alone ( alone patterns strain , . . Most approaches use a combination of shape shape of combination a use approaches Most . Furthermore, in contrast to earlier suggestions earlier to in contrast Furthermore, the relative response of single head regions regions head single of response relative the
is absent in in absent is 4)
in the case of the mayfly the of case the in
ih o paet rn dsenbe for discernible trend apparent no with
sported sported e variation variation e et al. et
to these approaches is their use of of use their is approaches these to
In contrast, In
oclypeal and the subgenal regions regions subgenal the and oclypeal (or the respective ridges) and the the and ridges) respective the (or , 2014; Martín 2014; ,
Siphlonurus in more d more in s .
tan o ec o the of each for strain This many to one mapping of of mapping one to many This
and the strain patterns are are patterns strain the and (Alfaro (Alfaro compare compare
the istantly related species species related istantly ) , et al. et eye although although
- are
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This article isThis article by protected copyright. All rightsreserved. Accepted predicted. the for account correctly to order in necessary is techniques, optimization other or MDA using FEA, for forces input the of modelling (whi sensory modified example for accommodate to environments adaptive altered to response in shape biting for relevant head substructures morphological general the or endoskeleton, the the for explanation an be could dyna the that suggest We uptake systems. food of evolution mechanical the of differences) principal (and principles common reveal to order in vertebrates, and insects as such groups organismal different Article across example for covariations, assessmen larger of context the in valuable especially is aspect This detectable. uptake food as ho unclear by accompanied detect to suited multidimensional the account into takes low i.e. calculations), lever as (such structure given a of component one only characterizing parameters biomechanical with detect to difficult instances these In insects. across phenomena frequent are can tentorium or orientation head general of changes that emphasized be to has It morphologies. head different significantly with h lo iey influence likely also ch
.
Optimizations which are not apparent by shape analysis alone alone analysis shape by apparent not are which Optimizations o mrhlgcl tutrs n more in structures morphological how mic concerted responses of single head regions to biting to regions head single of responses concerted mic mology for substructures) for mology d
even occur within insect orders (e.g in mayflies in (e.g orders insect within occur even ed asl shape capsule head frequent frequent
forces during feeding, otherwise erroneous strain patterns will be be will patterns strain erroneous otherwise feeding, during forces shifts of morphologies such as the mouthpart orientation, orientation, mouthpart the as such morphologies of shifts set o a of aspects - dimensional mechanical determinants. In contrast, FEA contrast, In determinants. mechanical dimensional - chewing, head morphologies as a whole can change change can whole a as morphologies head chewing, ).
It has to be stressed however, that accurate accurate that however, stressed be to has It adapt to similar biomechanical challenges biomechanical similar to adapt in
functional system and therefore might be be might therefore and system functional insects. Through concerted changes of of changes concerted Through insects.
distantly related taxa (probably even even (probably taxa related distantly
functional optimizations optimizations functional (Staniczek, 2001) (Staniczek, ts of shape of ts should should - chewing loadings loadings chewing therefore might be be might - function function organs organs ) and and )
such such
be
This article isThis article by protected copyright. All rightsreserved. comp of dynamics Evolutionary 2004. P.C. Wainwright, & D.I. Bolnick, M.E., Alfaro, 2005. C. Law, & B. Gevici, J., Ahrens, References interest of conflict no have they declare The authors interest of Conflict We interests Competing manuscript. Dutel Hugo especially of specimens again here used were which studies earlier sincerel are Cologne) University, Sport Koenig) Alexander Reumont von Beckmann Felix nano the during help for Schmitz Helmut and Schmitz Anke thank We Accepted Article Acknowledgements
have no competing competing interests no have Org. Evol. four usingthe biomechanical systems: anexample visualization.
Siphlonurus lacustris Siphlonurus
Uiest o Leipzig) of (University (Helmholtz Centre Geesthacht) Centre (Helmholtz
for help during the SRµCT experiments. Sina David and Johannes Funken (German (German Funken Johannes and David Sina experiments. SRµCT the during help for
58
: 495
Butterworth for useful discussions during the analyses and the preparation of the the of preparation the and analyses the during discussions useful for – 503.
. We thank the lab members lab the thank We .
- Heinemann, Burlington, NJ. Burlington, Heinemann, ad uan Düngelhoef Susanne and , y thanked for their help during bite force measurements in in measurements force bite during help their for thanked y
for validation for , Karen Meusemann Karen , aaiw a end an Paraview:
. Arnold Staniczek is thanked for providing providing for thanked is Staniczek Arnold .
of the MBE group at Hull University Hull at group MBE the of
-
(U bar mechanism. mechanism. bar (Zoological Research Museum Museum Research (Zoological niversity of Freiburg) of niversity - -
user tool for large data data large for tool user indentation experiments and experiments indentation Evol. Int. J. J. Int. Evol. , Björn M. Björn , lex
This article isThis article by protected copyright. All rightsreserved. Accepted Potthas J., Funken, S., David, of modeling Musculoskeletal 2016a. A. Blanke, & W. Potthast, J., Funken, S., David, rapid skulls: damselfish of function and Form 2009. M.W. Westneat, & W.J. Cooper, Imperfect 2014. R.S. Mehta, & P.C. Wainwright, M.E., Alfaro, J.S., Reece, D.C., Collar, feed the to relation in anatomy The 1962. P.J. Chisholm, 2007. G. Malacarne, & S. Fenoglio, T., Bo, Computational 2017b. M.J. ArticleBlank Fagan, & R. Holbrey, P.J., Watson, A., Blanke, Form 2017a. M.J. Fagan, & H. Dutel, A., Patera, H., Schmitz, A., Blanke, & F. Beckmann, R., Mokso, C., Greve, A., Blanke, 2014. X.K. Yang, & S.Q. Ge, F., Friedrich, R.G., Beutel, Fitness. and Performance Morphology, 1983. S.J. Arnold, mechanical linkages: and Levers 2014. S.N. Patek, & T. Claverie, P.S.L., Anderson, , . Wplr B, esh H, oh M, ekan F, etl R., Beutel, F., Beckmann, M., Koch, H., Letsch, B., Wipfler, A., e, under an evolutionary perspective: deciphering the role of single muscle muscle single of role the deciphering insects. related in closely regions perspective: evolutionary an under single of role the evolutionarycontext. an in muscles understanding to aid an as system mandible dragonfly the 9 niches. trophic of number limited a into evolution repeated and eels. moray in durophagy to transitions c in changes variable convergence: morphological 55 Plecoptera. other and Perlidae) (Plecoptera, Curtis Italy). marginata (northwestern stream class="italic">Perla Apennine an Entomol. (Insecta). Ephemeroptera and Odonata Palaeoptera of Revival Sci. evolution. head insect on view our changes biomechanics Interface Soc. of dragonfly analysis in relationships convergence formal including Anisoptera characters. morphological of phylogeny Phylogeny trade : – 24. 101.
284 -
offs inapower
: 20162412.
139 . De Gruyter, Berlin. . DeGruyter, : 358
14 : 20161038. – 364.
- amplified system. system. amplified
— t, W. & Blanke, A. 2016b. 2016b. A. Blanke, & W. t, head characters support a monophyletic origin of of origin monophyletic a support characters head Syst. Entomol. Syst. mandibles under an evolutionary perspective. perspective. evolutionary an under mandibles
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Carnivoran the of Performance Locomotor Forelimb. and Evolution Morphological 71 morphology. functional jaw on oral evolution body shape functional and diversity morphological performance. of study simulation a fishes: stream Physiol. co surae triceps voxel to structures. skeletal wrapping muscle of application cuticle. of insect properties Brunner. ineris, var. Pall., Biol. J. Exp. beetles. stag metallifer Cyclommatus in dimorphism force bite of determinants Homarus Lobster the of Exoskeleton americanus. The Organization: Hierarchical with Fiber Biological a of Mechanics the on Principles Serra, A., Figueirido, B. & B. Figueirido, A., Serra, : 2219 : 763 1 - : 1 . Scs C, rgeo PR & ab, . 2009 D. Raabe, & P.R. Triguero, C., Sachs, O., – – – 512 (Pt2) 512 2229. 767. 334. PLoS ONE , esmn, . Ptr, .. Dnt, . Myr C., Mayer, A., Donath, R.S., Peters, K., Meusemann, ., 22 itio and Multiscale Simulations: The Example of Lobster Cuticle. Cuticle. Lobster of Example The Simulations: Multiscale and itio 217 Adv. Mater. Adv. J. Morphol. J. : 519 : 1065 mplex architecture in man: implications for muscle function. function. muscle for implications man: in architecture mplex : 603 – Biomech. Model.Mechanobiol. Biomech. 526. 9 – . 1071. – 614. 21 270 J. Zool. Soc. India Palmqvist, P. 2014. A Three A 2014. P. Palmqvist, Ann. Société Entomol. Fr. Entomol. Ann. Société : 391 Acta Biomater. Acta : 976 – 400. – 983. L.V. & Aerts, P. 2014. Biomechanical Biomechanical 2014. P. Aerts, & L.V. - Performance Biological Composites Composites Biological Performance 7 - 13 : 2935 based finite element models of of models element finite based : 34 E LA LARVE DE NEMOURA NEMOURA DE LARVE LA E – – 11 49. - 2942. Based Composite Material Material Composite Based 4 : 35 : 91. - . Influence of Structural Structural of Influence . Dimensional Analysis of of Analysis Dimensional Fagan, M.J. 2012. The The 2012. M.J. Fagan, – Evol. Int. J. Org. Evol. J. Org. 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Oliver, der Morpholog der evolution. Many 2017. ecological plasticity theavian in pelvic limb skeleton. Ger. carapace. turtle emydid the in variation morphological of patterns significance. 239 phylogenetic and morphology its (Ephemeroptera): Eintagsfliegen Tübingen. Universität der vergleichenden Phylogenie zur und Beitrag Anatomie Ein Oniscigastridae). Ephemeroptera: (Insecta: Org. Evol. fun and pressures selective Chloroperlidae). and Perlidae (Plecoptera: Auriculari a skulls: crocodilian Morphol. extant approach. modeling element in finite and morphometric performance geometric combined mechanical and occupation toone. many is to function form of themapping when MaJ. experiments. indentation sensing displacement and load using modulus elastic : 147 Figueroa, J.M.T. de. 2013. Adult feeding habits of three Perloidea species species Perloidea three of habits feeding Adult 2013. de. J.M.T. Figueroa, 114 ter. Res. : 213 – 269 178. al. and Other Dermaptera. Dermaptera. Other and al. 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A.P., Bolnick, D.I., Bolnick, A.P., 35 133 : 99 McLachlan, 1873 1873 McLachlan, : 251 – 104. 274 – nd mayflies mayflies nd Evol. Int. J. J. Int. Evol. 300. Zoo ol Anz. Zool. : 483 8 : 122. l. Jena Jena l. - space space Karls – et al. et 495. J. - This article isThis article by protected copyright. All rightsreserved. Accepted measu parameter MPa. in values species The eyes. and (DTAs) arms tentorial 1 Table Table to application Articleand scaling, models, properties, tendon: and Muscle 1989. F.E. Zajac, J.C., Gee, S., Ho, R.G., Smith, H.C., Hazlett, J., Piven, P.A., Yushkevich, some of pressures and forces mandibular The 1989. M.E.G. Evans, & C.P. Wheater, & T. Siebert, K., Weißing, L., Reinhardt, T., Weihmann, Bellwood, P.C., Wainwright, 2005. C.D. Hulsey, & D.I. Bolnick, M.E., Alfaro, P.C., Wainwright, s and applied to the other species other the to applied and biomechanics andmotorcontrol. reliability. and efficiency improved significantly User Coleoptera predacious American the in Mandibles the Cockroach of Forces Bite and Biomechanics Powerful: complex biomechanical system. a in diversity of patterns fishes: labrid of skull the for morphospace functional Biol. Design? Organismal in Principle General A Function: to Form of Summary - 45 guided 3D active contour segmentation of anatomical structures: structures: anatomical of segmentation contour active 3D guided : 256 Please refer to the supplementary text S1 for further information on material material on information further for S1 text supplementary the to refer Please rements. of the d the of Periplaneta americana Periplaneta – 262. ifferent ifferent D.R., Westneat, M.W., Grubich, J.R. & Hoey, A.S. 2004. A A 2004. A.S. Hoey, & J.R. Grubich, M.W., Westneat, D.R., . Young’s modulus modulus Young’s J. Insect Physiol. values values . A Poisson’s ratio of 0.3 was assumed for all materials. materials. all for assumed was 0.3 of ratio Poisson’s A for the head and eye eye and head the for Biol. J. Linn. Soc. J. Linn. Biol. Crit. Rev. Biomed. Eng. Biomed. Crit. Rev. . PLoS ONE combinations used for the head capsule, dorsal dorsal capsule, head the for used combinations 35 : 815 10 NeuroImage : e0141226. – were measured for th for measured were 820. 82 Wipfler, B. 2015. 2015. B. Wipfler, : 1 – 25. Many 17 : 359 31 - : 1116 to – - Integr. Comp. Comp. Integr. 411. One Mapping Mapping One ree t al. et – 1128. Fast and and Fast dragonfly 2006. All This article isThis article by protected copyright. All rightsreserved. output. muscleforce to total relative contributions Table axis rotation insertion mandibular the and area attachment muscle the of surfa centroid capsule the head between the with surfaces eye right and left the of sum the dividing anterior forces reaction (FTC coefficients 2 Table F. auricularia F. P.marginata virens L. lacustris S. F. auricularia F. marginata P. lacustris S. virens L. AcceptedSpecies Article Species 3 o dorsal) (or Predicted forces in the mandibular adductor muscles of each species during biting and their their and biting during species each of muscles adductor mandibular the in forces Predicted Head width Head generated by the mandible joints the mandible generated by width width Head Head [mm] 3.12 8.03 5.23 2.01 =total BF/sum of left and right muscle forces muscle right and left of BF/sum =total JF) o ec species. each for (JRFs) 0.386 0.408 0.169 0.029 Head R wt te posterior the with JRF 7300 7300 7300 7300 7300 7300 7300 7300 7300 7300 7300 7300 (largest distance (largest L BF[N] 0.369 0.408 0.228 0.038 R total BF total 0.755 0.816 0.397 0.067 7300 7300 7300 7300 DTA 350 350 350 350 350 350 350 350 [N] 0.392 0.270 0.356 0.225 FTC in cluding eyes) cluding The JRF ratio was calculated by dividing the respective respective the dividing by calculated was ratio JRF The 4000 4000 4000 4000 4000 4000 4000 4000 0.53 0.39 0.42 0.42 Eye 350 350 350 350 L o ventral) (or MA as areference. 0.50 0.41 0.44 0.51 R L ant. L 0.23 0.33 0.33 0.08 , bite force (BF) predictions, force transmission transmission force predictions, (BF) force bite , L post.L R. h eye The JRF. 0.67 1.04 0.30 0.09 JRF[N] ), mandibular advantage (MA) and joint joint and (MA) advantage mandibular ), Rant. 0.29 0.52 0.35 0.09 Rpost. 0.65 0.81 0.34 0.10 - head ratio was obtained by by obtained was ratio head 0.33 0.32 1.10 0.82 JRFratio L 0.45 0.64 1.03 0.93 R ce. with 80 88 84 67 JAA[°] L A = JAA the 80 79 92 73 R virtual virtual head head Eye / / Eye ratio 0.08 0.09 0.71 0.46 axis axis This article isThis article by protected copyright. All rightsreserved. subgenal intern M.craniomandibularis 0md1, mandible; md, bite force; ridge; BF, SG, ridge; epistomal ER, corpotentorium; CT, arm; tentorial dorsal DTA, arm; tentorial sy each within (Odonata) Perla vectors (JRF) force reaction joint resultant and MDA the (b movement. mandible general and considered regions head the each for setup (MDA) species analysis dynamics multibody and regions head the of Overview 1 Fig. Figure Accepted Articleauricularia F. marginata P. virens L. lacustris S. Species marginata captions . (a) The head of of head The (a) . (e). Heads not to the same scale same the to not Heads (e). stem (Forficula & Perla: 2x; 2x; Perla: & (Forficula stem M. tentorio-mand.inf med. M. inf tentoriomand.lat. M. craniomand. internus M. tentorio-mand.sup med. M. sup tentorio-mand. lat. M. craniomand. Internus M. tentorio-mand.inf med. M. tentorio-mand.sup med. M. inf tentoriomand.lat. M. sup tentorio-mand. lat. M. craniomand. int M. tentorio-mand.inf med. M. tentorio-mand.sup med. M. inf tentoriomand.lat. M. sup tentorio-mand. lat. M. craniomand. internus M. (Plecoptera) Forficula auricularis Forficula Muscle (c), Siphlonurus Siphlonurus: 10x Siphlonurus: , JRFs have been scaled to aid visibility of JRF directions directions JRF of visibility aid to scaled been have JRFs , Muscle force [N] force Muscle 0.0466 0.0464 0.7920 0.0555 0.0555 1.3596 0.0302 0.0065 0.0175 0.0009 0.4929 0.0231 0.0033 0.0231 0.0033 0.0825 in ventral and dorsolateral view to illustrate to view dorsolateral and ventral in L lacustris 0.0475 0.0474 0.9471 0.0553 0.0555 1.4421 0.0352 0.0066 0.0205 0.0009 0.5029 0.0231 0.0033 0.0231 0.0033 0.1089 R for for (Ephemeroptera) ; Lestes: 5x) Lestes: ; Forficula %Muscle 89.5 96.1 89.9 17.1 17.1 61.0 L - 5.3 5.2 3.8 3.9 5.5 1.2 3.2 0.2 2.4 2.4 e) The mandible muscle setups for for setups muscle mandible The e) force . Abbreviations: ATA, anterior anterior ATA, Abbreviations: . auricularia us. 90.9 96.3 88.8 14.3 14.3 67.3 R 4.6 4.5 3.6 3.7 6.2 1.2 3.6 0.2 2.0 2.0 (d), and and (d), (Dermaptera) Lestes a part a virens (b), (b), of of This article isThis article by protected copyright. All rightsreserved. anter arm tentorial dorsal DTA, ( ridge); subgenal (including area genal/subgenal G/SG, ridge/area; to the of Comparison 4 Fig. c head. the of head of overview an regions head investigated of combinations possible all ratios (IQR) range Interquartile 3 Fig. appropriate. properties tentor dorsal the of properties material ( strains head view lateral and frontal in Siphlonurus (g+h) view. lateral in Perla (f) view. ventral and dorsal with D of half (lower view lateral in Forficula (d) view. ( capsule head each for (FEA) analyses element finite ( Results 2 Fig. including left Acceptedorpotentorium Article ridge head ior tentorial arm. tentorial ior side ɛ s 1), right side shows shows side right 1), . half transparent to provide internal lateral view). Left side shows shows side Left view). lateral internal provide to transparent half side n tnoim tutrs ewe te or species. four the between structures tentorium and connection to the head capsule); CT, corpotentorium; TENT, whole tentorium; ATA, ATA, tentorium; whole TENT, corpotentorium; CT, capsule); head the to connection All values are in microstrain, the position of the eyes is indicated with dashed lines where where lines dashed with indicated is eyes the of position the microstrain, in are values All most tensile principal strain ( strain principal tensile most half transparent to provide intern provide to transparent half ; Other ; Abbreviations: Abbreviations: region , remaining head regions head remaining ratios of ratios pairs ot compressive most ) A . TA Divisions show which head region was tested against other parts other against tested was region head which show Divisions interquartile ranges ranges interquartile , of the most tensile and most compressive stra compressive most and tensile most the of ial arms arms ial a nterior ɛ 1 . ) and eyes respectively eyes and al lateral view). (c) Forficula in dorsal and ventral ventral and dorsal in Forficula (c) view). lateral al & etra am; Tent. arms; tentorial rnia sris ( strains principal most compressive principal strain ( strain principal compressive most . (a+b) (a+b) . (see Material and Methods and Table S1 for for S1 Table and Methods and Material (see left (rIQRs) head head Lestes for all for side virens ɛ 3). FEA results are for actual actual for are results FEA 3). Abbreviations: ER, epistomal epistomal ER, Abbreviations: half transparent). (e) Perla in in Perla (e) transparent). half head region pairs associated associated pairs region head not for simulated alternative alternative simulated for not w , in frontal and lateral view view lateral and frontal in oe etru; CT tentorium; hole most tensile most ins ( ins ɛ ɛ 1 & & 1 3 ) principal principal ) of the of ) ɛ 3) for for 3) ( left , This article isThis article by protected copyright. All rightsreserved. combinations. material indica font Bold MPa). (350 tentorium dorsal and eyes “limp” SE, (350MPa); tentorium dorsal “soft” ST, MPa); (7300 tentorium dorsal “stiff” HT, arm; tentorial dorsal DTA, Abbreviations: (c) (Odonata); virens Lestes (b) (Ephemeroptera); lacustris Siphlonurus (a) strain. higher with structures for distribution each of numbers element different the for account to other Note strain. head overall on eyes and arms tentorial dorsal ( strains principal compressive Su ( the most tensile by separated pair region head each for ratios interquartile the of Overview S1: table Supplementary Supplementary Supplement Accepted Article S1 figure pplementary ary ary document material ɛ 1) and most compressive ( compressive andmost 1) el marginata Perla : Cumulative histograms of the distribution of most tensile and most most and tensile most of distribution the of histograms Cumulative : S1 : Additional ɛ 1 & 1 ɛ 3) to illustrate the influence of varying material varying of influence illustrate the 3) to methodological details methodological (Plecoptera); (d) Forficula auricularia (Dermaptera). (Dermaptera). auricularia Forficula (d) (Plecoptera); ɛ 1) strains. 1) that frequencies are relative to each each to relative are frequencies that and discussion. and structure. Small insets show strain strain show insets Small structure. properties of the of properties tes in vivo vivo in tes This article isThis article by protected copyright. All rightsreserved. Accepted Article This article isThis article by protected copyright. All rightsreserved. Accepted Article This article isThis article by protected copyright. All rightsreserved. Accepted Article This article isThis article by protected copyright. All rightsreserved. Accepted Article