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Grouping is a widespread form of predator defence, with individuals in groups often performing evasive collective movements in response to attack by predators. Individuals in these groups use behavioural rules to coordinate their movements, with visual cues about neighbours' positions and orientations often informing movement decisions. Although the exact visual cues individuals use to coordinate their movements with neighbours have not yet been decoded, some studies have suggested that stripes, lines, or other body patterns may act as conspicuous conveyors of movement information that could promote coordinated group movement, or promote dazzle camouflage, thereby confusing predators. We used phylogenetic logistic regressions to test whether the contrasting achromatic stripes present in four different taxa vulnerable to predation, including species within two orders of birds (Anseriformes and Charadriiformes), a suborder of Artiodac-tyla (the ruminants), and several orders of marine fishes (predominantly Perciformes) were associated with group living. Contrasting patterns were significantly more prevalent in social species, and tended to be absent in solitary species or species less vulnerable to predation. We suggest that stripes taking the form of light-coloured lines on dark backgrounds, or vice versa, provide a widespread mechanism across taxa that either serves to inform conspecifics of neighbours' movements, or to confuse predators, when moving in groups. Because detection and processing of patterns and of motion in the visual channel is essentially colour-blind, diverse animal taxa with widely different vision systems (including mono-, di-, tri-, and tetrachromats) appear to have converged on a similar use of achromatic patterns , as would be expected given signal-detection theory. This hypothesis would explain the convergent evolution of conspicuous achromatic patterns as an antipredator mechanism in numerous vertebrate species.
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Research
Cite this article: Negro JJ, Doña J, Blázquez
MC, Rodríguez A, Herbert-Read JE, Brooke M
de L. 2020 Contrasting stripes are a widespread
feature of group living in birds, mammals and
fishes. Proc. R. Soc. B 287: 20202021.
http://dx.doi.org/10.1098/rspb.2020.2021
Received: 17 August 2020
Accepted: 21 September 2020
Subject Category:
Evolution
Subject Areas:
evolution, behaviour, ecology
Keywords:
stripes, melanin, body patterns, collective
movement, antipredator defences, dazzle
Author for correspondence:
Juan J. Negro
e-mail: negro@ebd.csic.es
Electronic supplementary material is available
online at https://doi.org/10.6084/m9.figshare.
c.5136600.
Contrasting stripes are a widespread
feature of group living in birds, mammals
and fishes
Juan J. Negro1, Jorge Doña2,3, M. Carmen Blázquez4, Airam Rodríguez1,5,
James E. Herbert-Read6,7 and M. de L. Brooke6
1
Estación Biológica de Doñana-CSIC, Avda. Americo Vespucio 26, 41092 Sevilla, Spain
2
Illinois Natural History Survey, Prairie Research Institute, University of Illinois at Urbana-Champaign,
1816 S. Oak St., Champaign, IL 61820, USA
3
Departamento de Biología Animal, Universidad de Granada, Granada, Spain
4
Centro de Investigaciones Biológicas del Noroeste (CIBNOR), 23096 La Paz, Baja California Sur, Mexico
5
Grupo de Ornitología e Historia Natural de las Islas Canarias, GOHNIC, Canarias, Spain
6
Department of Zoology, University of Cambridge, Downing St, Cambridge CB2 3EJ, UK
7
Department of Biology, Aquatic Ecology Unit, Lund University, Lund 223 62, Sweden
JJN, 0000-0002-8697-5647; MCB, 0000-0002-0810-749X; AR, 0000-0001-7882-135X;
JEH-R, 0000-0003-0243-4518
Grouping is a widespread form of predator defence, with individuals
in groups often performing evasive collective movements in response to
attack by predators. Individuals in these groups use behavioural rules to
coordinate their movements, with visual cues about neighbourspositions
and orientations often informing movement decisions. Although the exact
visual cues individuals use to coordinate their movements with neighbours
have not yet been decoded, some studies have suggested that stripes, lines,
or other body patterns may act as conspicuous conveyors of movement
information that could promote coordinated group movement, or promote
dazzle camouflage, thereby confusing predators. We used phylogenetic
logistic regressions to test whether the contrasting achromatic stripes present
in four different taxa vulnerable to predation, including species within two
orders of birds (Anseriformes and Charadriiformes), a suborder of Artiodac-
tyla (the ruminants), and several orders of marine fishes (predominantly
Perciformes) were associated with group living. Contrasting patterns were
significantly more prevalent in social species, and tended to be absent in
solitary species or species less vulnerable to predation. We suggest that
stripes taking the form of light-coloured lines on dark backgrounds, or
vice versa,provide a widespread mechanism across taxa that either serves
to inform conspecifics of neighboursmovements, or to confuse predators,
when moving in groups. Because detection and processing of patterns and
of motion in the visual channel is essentially colour-blind, diverse animal
taxa with widely different vision systems (including mono-, di-, tri-, and
tetrachromats) appear to have converged on a similar use of achromatic pat-
terns, as would be expected given signal-detection theory. This hypothesis
would explain the convergent evolution of conspicuous achromatic patterns
as an antipredator mechanism in numerous vertebrate species.
1. Introduction
Group living characterizes the lives of many animals including flocking birds,
schooling fishes, and herding ungulates. Grouping is often a defensive strategy
to reduce the likelihood of individuals being attacked through detection,
dilution, confusion, or self-herd effects [14]. Because isolated individuals are
more likely to be targeted by predators [58], individuals in groups often
move to maintain cohesion by escaping from predators in the same direction
as other group members [9,10]. Many models aimed at explaining such
© 2020 The Author(s) Published by the Royal Society. All rights reserved.
coordinated movements assume animals rely primarily on
visual information to infer neighboursmovements and
positions [11], although the mechanosensory lateral line
system may also play a role in communication among
social fishes [12,13]. These assumptions seem appropriate
considering that birds are highly visually oriented animals
[14,15], and many fishes and mammals similarly rely on
vision when interacting with conspecifics [16].
Because vision appears essential for many species relying
on coordinated and cohesive escape from predators, particu-
lar visual cues may be used by social animals to promote
coordination. Numerous grouping species display conspicu-
ous stripes on their bodies (figure 1), with differences in
design related to their particular body plans. In mammals
and fishes, the majority of which have elongated bodies
parallel to the substrate, stripes often run parallel to the longi-
tudinal axis of the body. In birds, contrasting lines are often
displayed in open wings. In all groups, stripes are typically
achromatic. Light-coloured lines, often pure white, appear
on an otherwise darker (i.e. melanized) plumage. Brooke
[17] found that flocking shorebirds tended to have white
wing stripes, while solitary species did not, and suggested
that these white marks could provide a conspicuous flash
to other group members promoting cohesive take-off, or
could aid in coordinated movement. In such species, a role
of sexual selection as a driver of such body patterns may be
dismissed, as these marks are shown year-round by both
males and females in otherwise sexually dichromatic species
that display both breeding and non-breeding plumages [17].
Whether the stripes in other social taxa, in particular the con-
trasting bands on the bodies of some social mammals, such as
gazelles [18], or the stripes of different species of fish [1922]
play a role in coordination remains unclear.
Others have suggested that such body stripes, when com-
bined in a moving group, may produce dazzlepatterns that
could reduce either the likelihood of predators attacking or
their attack success rates [6,7,23]. Contrasting stripes or
lines have been hypothesized to provide camouflage or func-
tion to startle predators when they are suddenly displayed by
fleeing prey [7,24,25,26]. Dazzle patterns may also reduce the
ability of a predator to judge the speed and direction of their
prey [27]. Although there are no empirical data from wild
animals, computer simulations using humans as model
predators suggest that striped targets are among the most
difficult to capture. Nonetheless, simpler patterns, such as
all-grey colourations, are equally difficult to catch, and thus
evidence that stripes play an adaptive role in dazzle pattern-
ing remains inconclusive [27]. Earlier studies comparing
dorsal patterns of snakes concluded that longitudinal stripes
tended to occur in species with antipredator strategies favour-
ing fast escape over active defence (e.g. [28]). On the other
hand, garter snakes (Genus Tamnophis) display highly contrast-
ing longitudinal stripes and include the most social snakes,
with communal hibernation and mating [29]. These investi-
gations in reptiles already point to potential links between
striped patterns and both antipredator and social behaviour.
Expanding on Brookes [17] original idea for shorebirds,
here, we separately analyse colouration data on shorebirds,
waterfowl, ruminants, and fishes, while controlling for
phylogeny, to assess whether social species are more likely to
display stripes on their bodies and investigate their possible
function.We posit that social species may use contrastingstripes
to aid in coordinated movement or dazzle predators during
coordinated movement. According to these hypotheses, we pre-
dicted that for any given taxa, contrasting stripes should be
more prevalent in group-living species than in solitary ones.
Here, we test this prediction in species that rely on group cohe-
sion when fleeing from attacking predators, including herding
ungulates, flocking birds, and schooling fishes.
2. Material and methods
(a) Study species
We selected three different vertebrate taxa: two orders of
birds (shorebirds within Charadriiformes, and waterfowl
(Anseriformes)), one suborder of mammals (Ruminantia), and
fishes in the community of the Eastern Tropical Pacific Ocean
Figure 1. Species of birds, mammals, and fishes with examples of contrasting
stripes. From left to right, and top to bottom: Mallard Anas platyrhynchos,
including both males and females; northern shoveler Spatula clypeata;
common oystercatcher Haematopus ostralegus; black-tailed godwit Limosa
limosa; springbok Antidorcas marsupialis; dorcas gazelle Gazella dorcas. In the
fish picture: with longitudinal stripes, spottail grunts Haemulon maculicauda,
and with vertical stripes, Panamic sergeant major Abudefduf troschelii. Credits:
birds and mammals; Juan J. Negro. Fish picture: Christopher Swann.
royalsocietypublishing.org/journal/rspb Proc. R. Soc. B 287: 20202021
2
with species in the Orders: Anguilliformes, Clupeiformes,
Beloniformes, Perciformes, Scombriformes, and Istiophori-
formes, all of which include species which have contrasting
achromatic stripes (i.e. dark and light lines) (figure 1), as well
as other species with no such patterns. We investigated two
large bird groups where the presence/absence of wing marks
had caught the attention of previous researchers (i.e. [17] for
shorebirds and [30] for Anseriformes). In these bird groups,
stripes are only exposed in flight, and thus potentially when
the individuals attempt to escape from a predator. Both shore-
birds and ducks are more vulnerable and exposed to a large
set of predators when on land or on the water. In those situ-
ations, camouflage may be used to remain undetected (with
stripes being hidden), but when detected by predators, stripes
become exposed during flight. Mammals and fishes are different
in that they do not have foldable limbs, with stripes being perma-
nently visible. For these groups, we studied the most prominent
stripes; longitudinal stripes in mammals, and both longitudinal
and vertical stripes in fishes. The latter were analysed separately
as previous studies reported that stripe orientation in fishes is
linked to body shape [19], and to different ecological and behav-
ioural traits (e.g. [21]). The taxa under investigation included
both solitary and social species that often forage or rest in
groups. In these taxa, individuals that detect the predator or
are attacked often increase their speed during escape
movements, alerting others of the predators attack [31,32].
(b) Charadriiformes
We used the same dataset and speciesecological attributes as
Brooke [17] who assessed the occurrence of stripes in shorebirds
(excluding gulls, auks, and allies). Our study included 205
species in this order; although Brookes previous study included
210 (we excluded five species unavailable in the taxonomy
offered in BirdTree, see below). Brooke investigated several eco-
logical variables, such as migration, habitat, feeding technique,
and flocking behaviour and found that only flocking behaviour
was related to the presence of stripes on the wings. For our analy-
sis, we included (a) whether the species was mainly migratory or
sedentary, as the marks might help in group formation during
migration trips, (b) whether the species tended to form flocks
or was mainly solitary, and (c) wing-chord length as a proxy
for overall size. For flocking behaviour, Brooke [17] followed
Hayman et al. [33] and classified species as non-flocking if
terms such as singlyor in small groupswere used in their
respective descriptions. Species were classified as flocking if the
term flockwas used, or if groups exceeding 20 birds were men-
tioned. Our response variable was the presence/absence of white
lines on the wings (1 present, 0: absent). We did not analyse
patches on the tails and rumps that were not significantly
linked to sociality in Brookes [17] previous study.
(c) Anseriformes
To capture the difference in stripe expression that we knew a
priori distinguished the smaller ducks from the larger geese
and swans [34] we included 148 representative members of all
families of waterfowl (this order comprises 180 species in
total). We used a binomial response variable indicating the
presence or the absence of contrasting stripes on the wings
following Hegyi et al. [30]. In particular, we unified their scores
of 1, 2, and 3 into a single score, i.e. 1 = presence of white
patch in the wings, 0 = absence of white patch. Hegyi et al. [30]
did not include geese and swans (Anserinae) in their analyses,
as these species rarely have wing patches. For the few species
that do present white wing patches, we scored flying birds as dis-
played in the identification guide of Madge and Burn [35], and
followed a similar procedure to Hegyi et al. [30] as described
above. For species that are predominantly white, like some
swans, elongated dark patches on the wings were scored as
presence of stripes.
In contrast to the other taxa included in this study, a majority
of the species of Anseriformes are highly social during at least
part of their annual cycle. Therefore, for this order, we could
not distinguish between solitary or social species. As an explana-
tory variable, therefore, we used body mass as a proxy for body
size, and a binomial variable indicating if the species is migratory
or resident (again to assess whether marks might assist group
formation during migrations). We predicted that wing marks
would be associated with smaller ducks that are often hunted
in the air by falcons, whereas these lines should be largely
absent in the larger geese and swans that are rarely hunted by
aerial predators. The different susceptibility to predation accord-
ing to size affects their flying behaviour: ducks rank among the
faster flyers among birds and tend to fly in dense flocks, whereas
geese and swans fly with a lower flapping rate and usually adopt
v-flight formations [36].
Given the sexual dimorphism in many Anseriformes and the
absence of sexual differences in wing patch expression [30], we
selected male body mass to increase variation ( female body
mass produced similar resultsnot shown). Body mass data
were taken from Figuerola & Green [34]. The migratory status
of the species was taken from the distribution maps of the identi-
fication guide by Madge & Burn [35]. For partially migratory
species, we classified the species as migratory if the area of
breeding range abandoned in winter was larger than the resident
breeding area (present all year around).
(d) Ruminantia
Many species within the Artiodactyla, to which Ruminantia
belong, have linear contrasting stripes on their flanks and
dorsum (i.e. narrow bands or stripes differing in colour from
the surface on either side of them). Some species may have
other markings of different shapes (i.e. linear or not) on their
legs, rump, and faces. Caro & Stankowich [18] previously charac-
terized the presence and absence of contrasting marking in
different body parts in 198 species of artiodactyls and investi-
gated their function. Here, we built our own dataset to assess
whether the longitudinal stripes on the flanks of Ruminantia
are related to their degree of sociality. Similar to above, and
to remain consistent, we recorded the presence or absence of
longitudinal stripes on the bodies of animals as a binary response
variable, given the definition of a longitudinal marking by
Caro & Stankowich [18] as a stripe in both flanks contrasting
in colouration with the belly below and the dorsum above. Mam-
mals may also have vertical stripes, as with the patterning of
zebras, but in the Ruminantia that we studied (e.g. Tragelaphus
species) these are very narrow and faint lines that possibly
serve to provide crypsis [18], and therefore were not considered
in our analysis. Social species were defined as the ones forming
herds including more than one parentoffspring unit or more
than three unrelated individuals. Conversely, solitary species
are defined as the ones in which individuals tend to live alone
or in parentoffspring units. Smaller markings on other body
parts (i.e. legs, neck, or head) were not considered in the present
study, although they may serve a similar function. Body size data
were obtained from Smith et al. [37].
(e) Fishes
We selected representative species of the main Class of fishes, the
Actinopterygii. Among them, we chose species from the fish
community of the Eastern Tropical Pacific Ocean, following the
guide by Allen & Robertson [38] and the online-actualized
version https://biogeodb.stri.si.edu/sftep/en/pages. Because
many tropical species of fish can be colourful, we chose species
with several patterns, including species that were both striped
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3
and unstriped on the sides of their body. We analysed vertical
and horizontal lines separately, as they have been suggested
to convey different visual information, or relate to different life-
history traits and habitat features [19,21,22]. Our searching
criteria were as follows: first, and following the phylogenetic
order of the book, we identified species with some form of
stripe, either parallel to the horizontal axisi.e. horizontal
stripes or down the vertical axisi.e. vertical stripes (or bars as
in Seehausen et al. [21]). After this initial selection, we went
through our database, and for each species with vertical or
horizontal stripes, we randomly identified another species
within the same genus, or genus within the same family, that
did not have either of those stripes (plain species as in [22]). In
our final database of fishes, most species (90%) belonged to
the Perciformes, but with some representatives of additional
Orders (Clupeiformes, Beloniformes, Scombriformes, and
Istiophoriformes, and just two species of Anguilliformes). Finally,
and to align coherently with the other taxa in this study, we only
retained primary prey species (defined as species that remain
small enough to be eaten by larger fish throughout their lives),
and recorded as binary response variables the presence/absence
of one or more stripes (of any colour), and their sociality level
(i.e. solitary versus schooling). For assignment of sociality, we
followed the natural history notes of Allen & Robertson [38].
Some species are always in schools (sardines, mackerels),
others aggregate for migrations (and we included them as
schooling) and for others, especially the reef species, we con-
sidered them as social if the minimum size of groups reported
exceeded 50 individuals in any part of their life cycle.
3. Phylogenetic analysis
We tested whether the presence of stripes on the body corre-
lated with the evolution of group living, or other attributes
such as body mass or ecological characteristics, using phylo-
genetic logistic regression [3944]. In comparative analyses of
trait evolution, both completetrees (i.e. those that include
unsampled species using polytomy solvers) and sequenced
species onlytrees have their advantages and disadvantages
[45]. First, birthdeath polytomy resolvers used to infer
complete treesplace species onto trees randomly and inde-
pendently from the traits values, thus potentially breaking
down natural patterns of trait phylogenetic structure [46].
Similarly, sequenced species onlytrees, while not suffering
from this problem, contain fewer species that are potentially
non-randomly sampled, risking excluding their trait values
from analyses [45]. Accordingly, here we followed Upham
et al.s [45] recommendations and compared analyses run
on samples from both complete and sequenced-only trees
(see electronic supplementary material).
For each taxonomic group, we computed a 50% majority-
rule consensus tree using SumTrees v. 4.4.0 in DendroPy v.
4.4.0 [47,48] following the guidelines of Rubolini et al. [49]
to summarize individual gene trees for comparative studies.
By using this method, we obtained a single (optimal) consen-
sus tree for each group. According to Holder et al. [50], a 50%
majority-rule consensus tree can be seen as an optimal
summary of the posterior distribution of Markov Chain
Monte Carlo (MCMC) trees. We downloaded phylogenetic
subsets from broad phylogenetic syntheses. For the two
bird taxa, we used BirdTree ([51], http://birdtree.org). In par-
ticular, we downloaded phylogenetic trees from the Hackett
tree distributions (1000 trees from All species+ 1000 trees
from Sequenced speciesdistributions). For the Ruminantia
taxa, we used the species-level trees of extant Mammalia of
Upham et al. [45] (1000 trees from birthdeath node-dated
completed trees+ 1000 trees from birthdeath node-dated
DNA-onlydistributions). Lastly, for fish taxa, we downloaded
datafromthefishtreeoflife(100treesfromall-taxon
assembleddistributions plus the DNA-onlytime-calibrated
tree; [52]). The final consensuses complete treeswere com-
posed of 205 Charadriiformes, 148 Anseriformes, 197
Ruminantia, and 159 fish species, and the final consensuses
sequenced species onlytrees were composed of 144 Charadrii-
formes, 137 Anseriformes, 182 Ruminantia, and 120 fish species.
To assess whether stripes were associated with group-
living behaviour, we used phylogenetic logistic regression
analyses with the function phyloglm (logistic_MPLE method,
1000 independent bootstrap replicates, and p-values com-
puted using Wald tests) in the phylolm R package v. 2.6
[3944]. We evaluated model fit with binned residual
plotsspecifically, whether standard error bands from these
plots contain 95% of the binned residuals(binnedplot func-
tion from the arm v. 1.10-1 R package; [53]) and computing
an R
2
statistic suitable for statistical models with correlated
errors, such as the phylogenetic logistic regression models
used here (R2 function from the rr2 R package; [54]). Then,
we used the fitted coefficients from the phyloglm models to
plot the phylogenetic logistic regression curves using the
plogis function of the R package stats.
4. Results
We found significant associations between presence of stripes
and the level of sociality in all taxa that we investigated, and
these results were consistent across complete and sequenced-
only trees. Flocking Charadriiformes (shorebirds) were more
likely to have white wing stripes than non-flocking species
(phyloglm: R2
lik ¼0:26, p= 0.001; table 1, figures 2aand 3a).
Migratory status or body size (wing-chord length), however,
were not significantly related to the presence or absence
of wing markings ( phyloglm: migratory status, p= 0.599;
body size, p= 0.121; table 1). In Anseriformes (waterfowl),
most species of ducks had white wing stripes on dark
backgrounds, whereas most of the geese did not. In these
species, body mass was significantly correlated to the
presence or the absence of stripes, with smaller species
more likely to have stripes than larger ones (phyloglm:
R2
lik ¼0:18, p= 0.001; table 1, figures 2band 3b). Similar to
the Charadriiformes, migratory status was not related to the
presence or absence of wing stripes ( phyloglm: R2
lik ¼0:18,
p= 0.346; table 1). A model excluding the three seemingly
outlying data points (i.e. species with body mass greater
than 10 000 g) yielded essentially similar results (phyloglm:
R2
lik ¼0:12; body mass, p= 0.003; migratory status, p= 0.337).
Social species of ruminants were also more likely to have
stripes on the flanks than non-social species (phyloglm:
R2
lik ¼0:27; p= 0.003; table 1, figures 2cand 3c). Body mass,
however, was not related to the presence or the absence of
stripes (phyloglm: body mass, p= 0.133; table 1).
In fishes, sociality was associated with the presence or the
absence of horizontal stripes on the body, with social species
more likely to have horizontal stripes (phyloglm: R2
lik ¼0:37;
p< 0.001; table 1, figures 2dand 3d). Vertical lines (bars), how-
ever, were associated in the opposite direction to social species
royalsocietypublishing.org/journal/rspb Proc. R. Soc. B 287: 20202021
4
(i.e. social species were less likely to have vertical stripes; phy-
loglm: vertical stripes, R2
lik ¼0:16; p= 0.009; table 1).
Results for the subset of species for which actual sequence
data are available are given as electronic supplementary
material, and include phyloglm models (electronic sup-
plementary material table S1), and phylogenetic trees
(electronic supplementary material, figure S1).
5. Discussion
Stripes on the plumage, fur, and scales of prey species were
strongly associated with group living across taxa. While
different roles for the contrasting marks on animalsbodies
had previously been suggested in independent studies of
shorebirds, waterfowl, ruminants, and fishes [17,18,21,22,30],
evidence for their importance in social behaviour remained
inconclusive. In the all-social waterfowl, wing stripes were
relatedtothespeciesbody mass; a strong predictor of preda-
tion risk [55,56]. Given this, and given predation is a strong
driver of group living, we suggest these contrasting lines play
an important role in social antipredator defences of at least
three different vertebrate classes; mammals, birds, and fishes.
The finding that stripes are associated with social behav-
iour is even more striking considering the visual systems of
these taxa are known to vary widely. However, the combi-
nation of adjacent achromatic lines or bands mostly
black/dark and white (except in some fishes where structural
colours also play a role) suggests that colour perception is
not necessary for their role. Indeed, detection of patterns
and of motion is achieved by achromatic mechanisms, and
thus is essentially colour-blind [57]. These different taxa,
therefore, appear to have converged on a similar use of achro-
matic patterns, as would be expected given signal-detection
theory. Indeed, white bands with no pigment combined
with melanized areas may be generated by virtually any ver-
tebrate [58], and the stripes in the groups we studied were
indeed overwhelmingly monochromatic. Hence, these mark-
ings may be just as efficiently detected in either mono-, di-,
tri-, or tetra-chromatic species [5961], and visible in scotopic
conditions where most speciesvision becomes effectively
monochromatic owing to only rods remaining functional
[62]. It is noteworthy, however, that the species in our study
tend to live in open habitats. Anseriformes and Charadrii-
formes often live on open water, marshlands, and
coastlines, and the ruminants in our study tend to graze on
open grasslands [18]. Stoner et al. [63] also noted that artio-
dactyls with contrasting lines on their flanks were diurnal
and lived in open habitats. The fishes in our sample similarly
live in illuminated shallow waters. Hence, while nothing pre-
cludes that contrasting stripes remain functional both in full
daylight and in dim light conditions, detection of these
stripes is likely to be easier and more applicable to diurnal
species that live in relatively open habitats where contrasting
stripes are more conspicuous.
While the association between stripes and social behaviour
appears widespread, these markingsfunctional role remains
unresolved. Two primary (non-mutually exclusive) functions
have been proposed for these stripes. First, they could be
used by conspecifics to inform neighbours of rapid movement
and aid in coordinated movement [17], or second, to reduce
predation success through flash, dazzle, or confusion effects
[7,23]. In many cases of birds (including the Charadriiformes
and Anseriformes studied here) wing markings are often
only exposed when a bird takes flight, but remain hidden
when the bird folds its wings, with cryptic dorsal plumages
intended for background matching [7]. This sudden display
of contrasting lines has led authors to consider them primarily
as flash or dazzle marks destined to confuse an approaching
predator that might misjudge the speed or direction of the
preys escape [17]. While such an effect could also be achieved
by a single individual exposing its wings during its escape
flight, the flashes from multiple individuals would likely pro-
duce a stronger stimulus, and could hence be used by social
animals to reduce per capita predation risk. Indeed, because
predators prioritize distance estimation, their perception of
horizontal contours may be disrupted by such movements,
viewing such collectively moving prey as blurred images
[64]. There is also the suggestion that predators and prey may
have different systems for distance estimation and object recog-
nition, evidenced by their often different pupil shapevertically
elongated in ambush predators such as cats and vipers, and hori-
zontally elongated in prey species such as the Ruminantia [64].
Therefore, while stripes may confuse predators from long-
range, at short-range, these markings may inform individuals
of neighboursmotion, indirectly indicating to others the pres-
ence of a predator, and perhaps aiding in more coordinated
take-offs [17].
In contrast to the wing markings of birds that are only
exposed when birds fly, longitudinal lines of mammals and
fish are permanently visible. What roles do these markings
play in social behaviour? Caro & Stankowich [18] suggested
several functions for the stripes in Ruminantia, including pur-
suit deterrence, intraspecific signalling, and crypsis. In fishes,
some authors have suggested that stripes may disrupt the
body shape making it unrecognizable for predators [65] or
that stripes may make it difficult for a predator to focus on a
specific individual target [66]. Indeed, because visual acuity
scales with eye or body size in ray-finned fishes [67], larger
predatory species are more likely to be able to resolve stripes
than smaller shoaling species. This may suggest that stripes
are important in the confusion effect, horizontal lines serving
to reduce the ability of predators to judge the speed and direc-
tion of prey [23]. Denton & Rowe [20] further suggest that
stripes in the mackerel Scomber scombrus help to coordinate
shoaling behaviour, because stripes are perceived differently
with changes in body orientation (although they referred
to the vertical stripes of the dorsal side of a fishs body). Once
again, therefore, the association of grouping with these stripes
suggests that both confusion and coordination effects may play
an important role for these species. Further studies on the func-
tional role of horizontal and vertical stripes are clearly
warranted.
In fishes, however, we found opposite trends in relation to
whether horizontal (longitudinal) or vertical (bars) stripes
were associated with social behaviour. Shoaling fishes were
less likely to have vertical stripes, but more likely to have
horizontal stripes. These findings are consistent with other
studies, where open-water cichlids that engage in shoaling
behaviour tend to have horizontal stripes [21], whereas
cichlids that engage in aggressive territory defence are
likely to have vertical stripes [6871]. Moreover, the presence
of a horizontal stripe is thought to reduce aggressiveness in
neotropical and West African riverine cichlids [6971]. And
while neither vertical nor horizontal stripes were associated
with social behaviour in butterflyfishes, diagonal stripes
royalsocietypublishing.org/journal/rspb Proc. R. Soc. B 287: 20202021
5
were negatively correlated with butterflyfishesshoaling
tendencies [22]. Our wider taxonomic analysis, therefore,
appears largely consistent with previous research document-
ing both positive and negative effects of differently orientated
stripes on social behaviour. Indeed, Barlow [19] previously
concluded that stripes and bars act as both social signals
and antipredator adaptations in fishes.
While our result confirms many social species have
stripes and contrasting marks, there are species which form
large moving groups in open environments without any
(a)
(b)
Figure 2. Trait plots depicting the distribution of contrasting stripes (coloured traits) across the phylogeny of shorebirds (Charadriiformes, (a), grey), Anseriformes
((b), orange), Ruminants ((c), brown), and Fishes ((d), blue).
royalsocietypublishing.org/journal/rspb Proc. R. Soc. B 287: 20202021
6
conspicuous contrasting markings. Indeed, the European
starling Sturnus vulgaris, that does not display visually con-
trasting patterns in the plumage [72], yet displays some of
the most coordinated and collective behaviour in the
animal kingdom [7377]. Clearly, stripes are not a prerequi-
site for coordinated and cohesive movement. Similarly, the
presence of stripes is not entirely restricted to social species,
with some stripe patterns functioning as aposematic signals,
as in striped skunks Mephitis mephitis [78], or deimatic signals
that startle predators [26]. Stripes may also have other
functions, for instance, melanin-based plumage patches
have been suggested to signal dominance in social passerines,
(c)
(d)
Figure 2. (Continued.)
royalsocietypublishing.org/journal/rspb Proc. R. Soc. B 287: 20202021
7
with black patches located around the head and breast being
assessed during close encounters with conspecifics [79]. Also
in passerines, a study on leaf warblers (Phylloscopidae) with
varying widths of wing bars revealed that species with the
broader wing bars lived in darker habitats. Displaying
males, therefore, attempt to increase their conspicuousness
to competing conspecifics in darker environments [80].
Indeed, these species are solitary, and their contrasting
wing marks have evolved in contexts different to predation
avoidance or grouping. In addition, smaller head stripes in
numerous taxa may have evolved to conceal the eye, a promi-
nent structure in most species that may attract the attention of
predators or alert prey [24]. These eye stripes appear to be a
case of coincident disruptive camouflage [24,81] and would
therefore not be linked to increased sociality. Nevertheless,
while there are cases where social species have no stripes,
and cases where stripes serve multiple functions in animals,
our results suggest that all else being equal, social species
are more likely to have stripes than non-social species.
Using a comparative method where we accounted for phy-
logenetic signal, we found that contrasting and achromatic
stripes are more likely to be present across a broad taxonomic
range of social species that are often predated upon. It appears
that these stripes may aid in group coordination, or act to
increase the confusion effect, both of which may reduce per
capita predation risk. These achromatic patterns even suggest
that communication signals for alerting and recruiting others
may even work within mixed-species groups that are so
prevalent among social birds (including ducks and waders),
mammals (including gazelles), and fish [82]. Our work rep-
resents a rare example of aligned phenotypic characteristics
across a wide range of taxonomically diverse animals.
Data accessibility. All data needed to evaluate the conclusions in the
paper are present in the paper and/or the electronic supplementary
materials. Supplementary data (raw datasets) are available at Fig-
share (doi:10.6084/m9.figshare.12423623). An earlier version of the
manuscript was uploaded as a preprint in BioRxiv [83].
Authorscontributions. J.J.N. conceived the hypotheses, designed the
study, contributed to the dataset, and drafted the manuscript; J.D.
carried out the statistical analyses, helped in drafting the manuscript,
and prepared figures and supplementary material; M.C.B. contribu-
ted to the dataset and critically revised the manuscript; A.R.
contributed to the dataset and helped draft the manuscript. J.H.R.
refined hypotheses and helped draft the manuscript. M.B. contribu-
ted to the dataset and helped draft the manuscript. All authors
gave final approval for publication and agree to be held accountable
for the work performed therein.
Competing interests. We declare we have no competing interests.
Funding. A.R. was supported by Juan de la Cierva programme,
Spanish Ministry of Economy, Industry and Competitiveness (grant
no. IJCI-2015-23913). J.D. was supported by a Marie Curie Global
fellowship (grant no. 886532). J.E.H.-R. was supported by the
Whitten Lectureship in Marine Biology, and a Swedish Research
Council grant no. 2018-04076.
Acknowledgements. We thank Enrique Figueroa-Luque for his help in
building the dataset for mammals, and Christopher Swann for the
fish picture. Three anonymous reviewers greatly helped to improve
the first version of the manuscript.
0 5000 10 000 15 000
male body mass (g)
0
0.2
0.4
0.6
0.8
1.0
socialit
y
−3 −2 −1 3210
−3 −2 −1 3210
socialit
y
−3 −2 −1 3210
0
0.2
0.4
0.6
0.8
1.0
flocks
presence of stripes presence of stripes
(a)(b)
(c)(d)
Figure 3. Phylogenetic logistic regression curves predicting the presence or absence of contrasting stripes as a function of the flock size in Charadriiformes((a),
grey), body size in Anseriformes ((b), orange), sociality in Ruminants ((c), brown), and sociality in Fishes ((d), blue). Individual points are horizontally and vertically
jittered to improve visualization.
royalsocietypublishing.org/journal/rspb Proc. R. Soc. B 287: 20202021
8
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... Colouration can also provide physiological advantages, providing temperature regulation based on habitat type or season (Caro, 2005). The dorsum of mammals may be characterized by a variety of patterns, ranging from agouti, to spotted to banded or striped (Ancillotto & Mori, 2017;Negro et al., 2020). ...
... This significant negative correlation between age and contrast may indicate that the dorsal stripe plays a part in the color advertisement of young animals. As a semigregarious species, it is possible that if the stripe is intraspecifically visible, group members may better be able to monitor directional movement of young animals (Negro et al., 2020). The more contrasting stripe on animals F I G U R E 3 Representation of the significant difference between the contrast ratio of thoracic and lumbar regions of the dorsal stripe, and thus overall length, and season for an adult male Javan slow loris in the ( of smaller body size may also allow them to appear even large to both predators and conspecifics (Lai et al., 2008;Leone et al., 2019), such as seen in Neotropical possums (Monodelphis spp), where the presence of dark stripe on smaller individuals decreased detection and predation (Leone et al., 2019). ...
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Article
In mammals, colouration patterns are often related to concealment, intraspecific communication, including aposematic signals, and physiological adaptations. Slow lorises (Nycticebus spp.) are arboreal primates native to Southeast Asia that display stark colour contrast, are highly territorial, regularly enter torpor, and are notably one of only seven mammal taxa that possess venom. All slow loris species display a contrasting stripe that runs cranial-caudally along the median sagittal plane of the dorsum. We examine whether these dorsal markings facilitate background matching, seasonal adaptations, and intraspecific signaling. We analyzed 195 images of the dorsal region of 60 Javan slow loris individuals (Nycticebus javanicus) from Java, Indonesia. We extracted greyscale RGB values from dorsal pelage using ImageJ software and calculated contrast ratios between dorsal stripe and adjacent pelage in eight regions. We assessed through generalized linear mixed models if the contrast ratio varied with sex, age, and seasonality. We also examined whether higher contrast was related to more aggressive behavior or increased terrestrial movement. We found that the dorsal stripe of N. javanicus changed seasonally, being longer and more contrasting in the wet season, during which time lorises significantly increased their ground use. Stripes were most contrasting in younger individuals of dispersal age that were also the most aggressive during capture. The dorsal stripe became less contrasting as a loris aged. A longer stripe when ground use is more frequent can be related to disruptive colouration. A darker anterior region by younger lorises with less fighting experience may allow them to appear larger and fiercer. We provide evidence that the dorsum of a cryptic species can have multimodal signals related to concealment, intraspecific communication, and physiological adaptations.
... Studies of motion dazzle markings have mostly focused on stripes or zigzag patterns, but other patterns such as circles (Hamalainen et al., 2015), and block markings (Santer, 2013) also have the role of motion dazzle. These markings were more likely to occur as the group size gets larger (Negro et al., 2020). The reason may be that such markings increase the "confusion effect", where the success of a predator's attack decreases as the size or density of the group increases, benefiting the individuals in the group. ...
... We assumed that it may indicate that white markings serve as an anti-predation strategy, motion dazzle, which may explain why the hindquarter markings of bovids were always conspicuous instead of being concealable. Contrasting body patterns promoting dazzle camouflage are widespread in group-living mammals (Negro et al., 2020), observations in lizards and experiment on computers have shown that dazzle markings tend to appear in smaller prey (Kodandaramaiah et al., 2020), it is therefore reasonable to assume that in large mammals of the bovid family, the evolution of dazzle markings are similarly related to the drive by the group size and body size. For example, the Tibetan gazelle Procapra picticaudata is endemic to the Tibetan Plateau, with a shoulder height of about 60 cm, often in groups of 2-10 individuals (Li, 2016). ...
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Conspicuous coloration in animals serves many functions such as anti-predation. Anti-predation strategies include motion dazzle and flash behavior. Motion dazzle markings can reduce the probability of being preyed on because the predators misjudge their movement. In flash behavior, prey demonstrate conspicuous cue while fleeing; the predators follow them, however the prey hide their markings and the predators assume that the prey has vanished. To investigate whether bovids use conspicuous hindquarter markings as an anti-predatory behavior, we undertook phylogenetically controlled analyses to explore under what physiological characteristics and environmental factors bovids might have this color pattern. The results suggested that rump patches and tail markings were more prevalent in bovids living in larger-sized groups, which supports the hypothesis of intraspecific communication. Moreover, we observed the occurrence of conspicuous white hindquarter markings in bovids having smaller body size and living in larger groups, suggesting a motion dazzle function. However, the feature of facultative exposing color patterns (flash markings) was not associated with body size, which was inconsistent with predictions and implied that bovids may not adopt this as an anti-predator strategy. It was concluded that species in bovids with conspicuous white hindquarter markings adopt motion dazzle as an anti-predation strategy while fleeing and escaping from being prey on.
... The VertLife database has two types of phylogenetic trees, a "complete" tree and a "sequenced species only" tree. Both types of trees provide different evolutionary relationships and tree topologies [22,23]. Therefore, we combined both types of trees to generate a maximum consensus tree. ...
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Glaucoma, an eye disorder caused by elevated intraocular pressure (IOP), is the leading cause of irreversible blindness in humans. Understanding how IOP levels have evolved across animal species could shed light on the nature of human vulnerability to glaucoma. Here, we studied the evolution of IOP in mammals and birds and explored its life history correlates. We conducted a systematic review, to create a dataset of species-specific IOP levels and reconstructed the ancestral states of IOP using three models of evolution (Brownian, Early burst, and Ornstein–Uhlenbeck (OU)) to understand the evolution of glaucoma. Furthermore, we tested the association between life history traits (e.g., body mass, blood pressure, diet, longevity, and habitat) and IOP using phylogenetic generalized least squares (PGLS). IOP in mammals and birds evolved under the OU model, suggesting stabilizing selection toward an optimal value. Larger mammals had higher IOPs and aquatic birds had higher IOPs; no other measured life history traits, the type of tonometer used, or whether the animal was sedated when measuring IOP explained the significant variation in IOP in this dataset. Elevated IOP, which could result from physiological and anatomical processes, evolved multiple times in mammals and birds. However, we do not understand how species with high IOP avoid glaucoma. While we found very few associations between life history traits and IOP, we suggest that more detailed studies may help identify mechanisms by which IOP is decoupled from glaucoma. Importantly, species with higher IOPs (cetaceans, pinnipeds, and rhinoceros) could be good model systems for studying glaucoma-resistant adaptations.
... It is thought that these stripes may serve to reduce intraspecific aggression while also concealing the fish from their prey during hunting [113]. This positive correlation between stripes and group interactions extends from fishes to birds and mammals [116], suggesting convergent evolution of this NCC derived trait. Microevolution in this trait can manifest through the presence and number of stripes, and we know much of the genetic basis of this trait from mutant and naturally-occurring variants in zebrafish [117]. ...
Article
Vertebrates have some of the most complex and diverse features in animals, from varied craniofacial morphologies to colorful pigmentation patterns and elaborate social behaviors. All of these traits have their developmental origins in a multipotent embryonic lineage of neural crest cells. This “fourth germ layer” is a vertebrate innovation and the source of a wide range of adult cell types. While others have discussed the role of neural crest cells in human disease and animal domestication, less is known about their role in contributing to adaptive changes in wild populations. Here, we review how variation in the development of neural crest cells and their derivatives generates considerable phenotypic diversity in nature. We focus on the broad span of traits under natural and sexual selection whose variation may originate in the neural crest, with emphasis on behavioral factors such as intraspecies communication that are often overlooked. In all, we encourage the integration of evolutionary ecology with developmental biology and molecular genetics to gain a more complete understanding of the role of this single cell type in trait covariation, evolutionary trajectories, and vertebrate diversity.
... Functional significance of the pigment pattern in nature is not well understood, though both wild and domesticated D. rerio attend to pattern variation in choosing shoalmates in the laboratory, and some spotted mutants can be preferred to the wild type [8][9][10]. Patterns of other teleosts function in mate choice, aggressive displays, avoidance of predation, and other behaviors [11][12][13][14][15]. Other species of Danio have stripes, spots, vertical bars and other patterns, and are similar to zebrafish in their amenability to genetic and developmental analyses [10,[16][17][18][19]. ...
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Vertebrate pigmentation is a fundamentally important, multifaceted phenotype. Zebrafish, Danio rerio, has been a valuable model for understanding genetics and development of pigment pattern formation due to its genetic and experimental tractability, advantages that are shared across several Danio species having a striking array of pigment patterns. Here, we use the sister species D. quagga and D. kyathit, with stripes and spots, respectively, to understand how natural genetic variation impacts phenotypes at cellular and organismal levels. We first show that D. quagga and D. kyathit phenotypes resemble those of wild-type D. rerio and several single locus mutants of D. rerio, respectively, in a morphospace defined by pattern variation along dorsoventral and anteroposterior axes. We then identify differences in patterning at the cellular level between D. quagga and D. kyathit by repeated daily imaging during pattern development and quantitative comparisons of adult phenotypes, revealing that patterns are similar initially but diverge ontogenetically. To assess the genetic architecture of these differences, we employ reduced-representation sequencing of second-generation hybrids. Despite the similarity of D. quagga to D. rerio, and D. kyathit to some D. rerio mutants, our analyses reveal a complex genetic basis for differences between D. quagga and D. kyathit, with several quantitative trait loci contributing to variation in overall pattern and cellular phenotypes, epistatic interactions between loci, and abundant segregating variation within species. Our findings provide a window into the evolutionary genetics of pattern-forming mechanisms in Danio and highlight the complexity of differences that can arise even between sister species. Further studies of natural genetic diversity underlying pattern variation in D. quagga and D. kyathit should provide insights complementary to those from zebrafish mutant phenotypes and more distant species comparisons.
... The reasons underlying different colouration in birds has been hotly debated for decades [17,34,35], although their variation may only be a reflection of the enormous colour space, or colour gamut, achieved by Class Aves [36] compared to the other land vertebrates, and mammals in particular [37,38]. As an example of within-genus colour diversity, the Monarcha species in the geographically restricted Solomon Islands differ most dramatically in plumage colouration than in any other morphological character [39,40]. ...
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The family Ciconiidae comprises 19 extant species which are highly social when nesting and foraging. All species share similar morphotypes, with long necks, bill and legs, and are mostly colored in the achromatic spectrum (white, black, black and white, or shades of grey). Stork may have, however, brightly colored integumentary areas in, for instance, the bill, legs or the eyes. These chromatic patches are small in surface compared with the whole body. We have analyzed the conservatism degree of coloration in 10 body areas along an all-species stork phylogeny derived from BirdTree using Geiger models. We obtained low conservativism in frontal areas (head and neck), contrasting with a high conservatism in the rest of the body. The frontal areas tend to concentrate the chromatic spectrum whereas the rear areas, much larger in surface, are basically achromatic. These results lead us to suggest that the divergent evolution of the coloration of frontal areas is related to species recognition through visual cue assessment in the short-range, when storks form mixed-species flocks in foraging or resting areas.
... Functional significance of the pigment pattern in nature is not well understood, though both wild and domesticated D. rerio attend to pattern variation in choosing shoalmates in the laboratory, and some spotted mutants can be preferred to the wild type [8][9][10]. Patterns of other teleosts function in mate choice, aggressive displays, avoidance of predation, and other behaviors [11][12][13][14]. Other species of Danio have stripes, spots, vertical bars and other patterns, and are similar to zebrafish in their amenability to genetic and developmental analyses [10,[15][16][17][18]. ...
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Vertebrate pigmentation is a fundamentally important, multifaceted phenotype. Zebrafish, Danio rerio , has been a valuable model for understanding genetics and development of pigment pattern formation due to its genetic and experimental tractability, advantages that are shared across several Danio species having a striking array of pigment patterns. Here, we use the sister species D. quagga and D. kyathit , with stripes and spots, respectively, to understand how natural genetic variation impacts phenotypes at cellular and organismal levels. We first show that D. quagga and D. kyathit phenotypes resemble those of wild-type D. rerio and several single locus mutants of D. rerio , respectively, in a morphospace defined by pattern variation along dorsoventral and anteroposterior axes. We then identify differences in patterning at the cellular level between D. quagga and D. kyathit by repeated daily imaging during pattern development and quantitative comparisons of adult phenotypes, revealing that patterns are similar initially but diverge ontogenetically. To assess the genetic architecture of these differences, we employ reduced-representation sequencing of second-generation hybrids. Despite the similarity of D. quagga to D. rerio , and D. kyathit to some D. rerio mutants, our analyses reveal a complex genetic basis for differences between D. quagga and D. kyathit , with several quantitative trait loci contributing to variation in overall pattern and cellular phenotypes, epistatic interactions between loci, and abundant segregating variation within species. Our findings provide a window into the evolutionary genetics of pattern-forming mechanisms in Danio and highlight the complexity of differences that can arise even between sister species. Further studies of natural genetic diversity underlying pattern variation in D. quagga and D. kyathit should provide insights complementary to those from zebrafish mutant phenotypes and more distant species comparisons. Author Summary Pigment patterns of fishes are diverse and function in a wide range of behaviors. Common pattern themes include stripes and spots, exemplified by the closely related minnows Danio quagga and D. kyathit , respectively. We show that these patterns arise late in development owing to alterations in the development and arrangements of pigment cells. In the closely related model organism zebrafish ( D. rerio ) single genes can switch the pattern from stripes to spots. Yet, we show that pattern differences between D. quagga and D. kyathit have a more complex genetic basis, depending on multiple genes and interactions between these genes. Our findings illustrate the importance of characterizing naturally occuring genetic variants, in addition to laboratory induced mutations, for a more complete understanding of pigment pattern development and evolution.
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Colour patterning in extant animals can be used as a reliable indicator of their biology and, in extant fish, can inform on feeding strategy. Fossil fish with preserved colour patterns may thus illuminate the evolution of fish behaviour and community structure, but are understudied. Here we report preserved melanin-based integumentary colour pattern-ing and internal anatomy of the fossil moonfish Mene rhombea (Menidae) from the Bolca Lagerst€ atte (Eocene (Ypresian), northeast Italy). The melanosome-based longitudinal stripes of M. rhombea differ from the dorsal rows of black spots in its extant relative M. maculata, suggesting that the ecology of moonfish has changed during the Cenozoic. Extant moonfish are coastal schooling fish that feed on benthic invertebrates, but the longitudinal stripes and stomach contents with fish remains in M. rhombea suggest unstructured open marine ecologies and a piscivorous diet. The localized distribution of extant moonfish species in the Indo-Pacific Ocean may reflect, at least in part, tectonically-driven reorganization of global oceanographic patterns during the Cenozoic. It is likely that shifts in habitat and colour patterning genes promoted colour pattern evolution in the menid lineage.
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Many nocturnal animals, including invertebrates such as scorpions and a variety of vertebrate species, including toadlets, flying squirrels, owls, and nightjars, emit bright fluorescence under ultraviolet light. However, the ecological significance of this unique coloration so attached to nocturnality remains obscure. Here, we used an intensively studied population of migratory red-necked nightjars (Caprimulgus ruficollis) to investigate inter-individual variation in porphyrin-based pink fluorescence according to sex, age, body condition, time of the year, and the extent of white plumage patches known to be involved in sexual communication. Males and females exhibited a similar extent of pink fluorescence on the under-side of the wings in both juvenile and adult birds, but males had larger white patches than females. Body condition predicted the extent of pink fluorescence in juvenile birds, but not in adults. On average, the extent of pink fluorescence in juveniles increased by ca. 20% for every 10-g increase in body mass. For both age classes, there was a slight seasonal increase (1–4% per week) in the amount of fluorescence. Our results suggest that the porphyrin-based coloration of nightjars might signal individual quality, at least in their first potential breeding season, although the ability of these and other nocturnal birds to perceive fluorescence remains to be unequivocally proven.
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Big, time-scaled phylogenies are fundamental to connecting evolutionary processes to modern biodiversity patterns. Yet inferring reliable phylogenetic trees for thousands of species involves numerous trade-offs that have limited their utility to comparative biologists. To establish a robust evolutionary timescale for all approximately 6,000 living species of mammals, we developed credible sets of trees that capture root-to-tip uncertainty in topology and divergence times. Our “backbone-and-patch” approach to tree building applies a newly assembled 31-gene supermatrix to two levels of Bayesian inference: (1) backbone relationships and ages among major lineages, using fossil node or tip dating, and (2) species-level “patch” phylogenies with nonoverlapping in-groups that each correspond to one representative lineage in the backbone. Species unsampled for DNA are either excluded (“DNA-only” trees) or imputed within taxonomic constraints using branch lengths drawn from local birth–death models (“completed” trees). Joining time-scaled patches to backbones results in species-level trees of extant Mammalia with all branches estimated under the same modeling framework, thereby facilitating rate comparisons among lineages as disparate as marsupials and placentals. We compare our phylogenetic trees to previous estimates of mammal-wide phylogeny and divergence times, finding that (1) node ages are broadly concordant among studies, and (2) recent (tip-level) rates of speciation are estimated more accurately in our study than in previous “supertree” approaches, in which unresolved nodes led to branch-length artifacts. Credible sets of mammalian phylogenetic history are now available for download at http://vertlife.org/phylosubsets, enabling investigations of long-standing questions in comparative biology.
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Detailed quantifications of how predators and their grouping prey interact in three dimensions (3D) remain rare. Here we record the structure and dynamics of fish shoals (Pseudomugil signifer) in 3D both with and without live predators (Philypnodon grandiceps) under controlled laboratory conditions. Shoals adopted two distinct types of shoal structure: “sphere-like” geometries at depth and flat “carpet-like” structures at the water’s surface, with shoals becoming more compact in both horizontal and vertical planes in the presence of a predator. The predators actively stalked and attacked the prey, with attacks being initiated when the shoals were not in their usual configurations. These attacks caused the shoals to break apart, but shoal reformation was rapid and involved individuals adjusting their positions in both horizontal and vertical dimensions. Our analyses revealed that targeted prey were more isolated from other conspecifics, and were closer in terms of distance and direction to the predator compared to non-targeted prey. Moreover, which prey were targeted could largely be identified based on individuals’ positions from a single plane. This highlights that previously proposed 2D theoretical models and their assumptions appear valid when considering how predators target groups in 3D. Our work provides experimental, and not just anecdotal, support for classic theoretical predictions and also lends new insights into predatory–prey interactions in three-dimensional environments.
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Many researchers want to report an R2 to measure the variance explained by a model. When the model includes correlation among data, such as phylogenetic models and mixed models, defining an R2 faces two conceptual problems. (i) It is unclear how to measure the variance explained by predictor (independent) variables when the model contains covariances. (ii) Researchers may want the R2 to include the variance explained by the covariances by asking questions such as "How much of the data is explained by phylogeny?" Here, I investigate three R2s for phylogenetic and mixed models. Rresid2 is an extension of the ordinary least-squares R2 that weights residuals by variances and covariances estimated by the model; it is closely related to Rglmm2 presented by Nakagawa and Schielzeth (2013). R2pred is based on predicting each residual from the fitted model and computing the variance between observed and predicted values. Rlik2 is based on the likelihood of fitted models and therefore reflects the amount of information that the models contain. These three R2s are formulated as partial R2s, making it possible to compare the contributions of predictor variables and variance components (phylogenetic signal and random effects) to the fit of models. Because partial R2s compare a full model with a reduced model without components of the full model, they are distinct from marginal R2s that partition additive components of the variance. The properties of the R2s for phylogenetic models were assessed using simulations for continuous and binary response data (phylogenetic generalized least squares and phylogenetic logistic regression). Because the R2s are designed broadly for any model for correlated data, the R2s were also compared for LMMs and GLMMs. Rresid2, Rpred2, and Rlik2 all have similar performance in describing the variance explained by different components of models. However, Rpred2 gives the most direct answer to the question of how much variance in the data is explained by a model. Rresid2 is most appropriate for comparing models fit to different datasets, because it does not depend on sample sizes. And Rlik2 is most appropriate to assess the importance of different components within the same model applied to the same data, because it is most closely associated with statistical significance tests.
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Far more species of organisms are found in the tropics than in temperate and polar regions, but the evolutionary and ecological causes of this pattern remain controversial1,2. Tropical marine fish communities are much more diverse than cold-water fish communities found at higher latitudes3,4, and several explanations for this latitudinal diversity gradient propose that warm reef environments serve as evolutionary ‘hotspots’ for species formation5,6,7,8. Here we test the relationship between latitude, species richness and speciation rate across marine fishes. We assembled a time-calibrated phylogeny of all ray-finned fishes (31,526 tips, of which 11,638 had genetic data) and used this framework to describe the spatial dynamics of speciation in the marine realm. We show that the fastest rates of speciation occur in species-poor regions outside the tropics, and that high-latitude fish lineages form new species at much faster rates than their tropical counterparts. High rates of speciation occur in geographical regions that are characterized by low surface temperatures and high endemism. Our results reject a broad class of mechanisms under which the tropics serve as an evolutionary cradle for marine fish diversity and raise new questions about why the coldest oceans on Earth are present-day hotspots of species formation.
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Animal camouflage has long been used to illustrate the power of natural selection, and provides an excellent testbed for investigating the trade‐offs affecting the adaptive value of colour. However, the contemporary study of camouflage extends beyond evolutionary biology, co‐opting knowledge, theory and methods from sensory biology, perceptual and cognitive psychology, computational neuroscience and engineering. This is because camouflage is an adaptation to the perception and cognition of the species (one or more) from which concealment is sought. I review the different ways in which camouflage manipulates and deceives perceptual and cognitive mechanisms, identifying how, and where in the sequence of signal processing, strategies such as transparency, background matching, disruptive coloration, distraction marks, countershading and masquerade have their effects. As such, understanding how camouflage evolves and functions not only requires an understanding of animal sensation and cognition, it sheds light on perception in other species. Camouflage provides an excellent testbed for investigating the trade‐offs affecting the adaptive value of colour. However, because camouflage is an adaptation to the perception and cognition of the species (one or more) from which concealment is sought, the study of camouflage sheds light on visual processing and decision‐making in other species. This review charts the rapid recent progress in understanding the different methods by which camouflage is achieved, within a framework of minimizing the signal‐to‐noise ratio. Photo credit: Gerard Cheshire
Book
Mixed-Species Groups of Animals: Behavior, Community Structure, and Conservation presents a comprehensive discussion on the mixed-species groups of animals, a spectacular and accessible example of the complexity of species interactions.