Collective decision-making appears more egalitarian in populations where group fission costs are higher

Abstract

Collective decision-making is predicted to be more egalitarian in conditions where the costs of group fission are higher. Here, we ask whether Trinidadian guppies (Poecilia reticulata) living in high or low predation environments, and thereby facing differential group fission costs, make collective decisions in line with this prediction. Using a classic decision-making scenario, we found that fish from high predation environments switched their positions within groups more frequently than fish from low predation environments. Because the relative positions individuals adopt in moving groups can influence their contribution towards group decisions, increased positional switching appears to support the prediction of more evenly distributed decision-making in populations where group fission costs are higher. In an agent-based model, we further identified that more frequent, asynchronous updating of individuals' positions could explain increased positional switching, as was observed in fish from high predation environments. Our results are consistent with theoretical predictions about the structure of collective decision-making and the adaptability of social decision-rules in the face of different environmental contexts.

Full text

royalsocietypublishing.org/journal/rsbl
Research
Cite this article: Herbert-Read JE, Wade ASI,
Ramnarine IW, Ioannou CC. 2019 Collective
decision-making appears more egalitarian in
populations where group fission costs are
higher. Biol. Lett. 15: 20190556.
http://dx.doi.org/10.1098/rsbl.2019.0556
Received: 29 July 2019
Accepted: 20 November 2019
Subject Areas:
behaviour, ecology, evolution
Keywords:
consensus, coordination, information,
Poecilia reticulata
Author for correspondence:
J. E. Herbert-Read
e-mail: james.herbert.read@gmail.com
Electronic supplementary material is available
online at https://doi.org/10.6084/m9.figshare.
c.4772591.
Animal behaviour
Collective decision-making appears more
egalitarian in populations where group
fission costs are higher
J. E. Herbert-Read1,2, A. S. I. Wade3, I. W. Ramnarine4and C. C. Ioannou3
1
Department of Zoology, University of Cambridge, Cambridge, UK
2
Department of Biology, Aquatic Ecology Unit, Lund University, Lund, Sweden
3
School of Biological Sciences, Bristol University, Bristol, UK
4
Department of Life Sciences, The University of the West Indies, St Augustine, Trinidad and Tobago
JEH-R, 0000-0003-0243-4518; CCI, 0000-0002-9739-889X
Collective decision-making is predicted to be more egalitarian in conditions
where the costs of group fission are higher. Here, we ask whether Trinida-
dian guppies (Poecilia reticulata) living in high or low predation
environments, and thereby facing differential group fission costs, make
collective decisions in line with this prediction. Using a classic decision-
making scenario, we found that fish from high predation environments
switched their positions within groups more frequently than fish from low
predation environments. Because the relative positions individuals adopt
in moving groups can influence their contribution towards group decisions,
increased positional switching appears to support the prediction of more
evenly distributed decision-making in populations where group fission
costs are higher. In an agent-based model, we further identified that more
frequent, asynchronous updating of individuals’positions could explain
increased positional switching, as was observed in fish from high predation
environments. Our results are consistent with theoretical predictions about
the structure of collective decision-making and the adaptability of social
decision-rules in the face of different environmental contexts.
1. Introduction
Collective decisions involve individuals in groups combining their own imper-
fect estimates of the world around them to reach consensuses about travel
directions, activities or choices while, at the same time, remaining cohesive
[1]. In many cases, if animals are to benefit from such information sharing,
they should distribute decision-making evenly between group members [1].
However, because conflict exists in groups, where individuals have to balance
the need for social cohesion with that of their own goal-oriented behaviour
[1–4], some individuals may disproportionally influence the decision-making
process, through either active or passive mechanisms.
Theoretical models suggest that the degree to which decision-making is
shared between group members is influenced by both environmental and
social conditions [5,6]. In environments where the benefits of remaining with
other group members outweigh any potential ‘consensus costs’, that is, costs
of following others’decisions, then equally shared decision-making is more
likely to evolve [7,8]. Unshared decision-making, on the other hand, is more
likely to evolve when consensus costs are relatively high compared with the
benefits of social cohesion [7,8]. Importantly, under both these scenarios, the
observed outcome of decision-making can often be the same, where groups
remain cohesive despite consensus being reached by relatively shared or
unshared decision-making processes.
© 2019 The Author(s) Published by the Royal Society. All rights reserved.

Investigating these theoretical predictions requires an
experimental system where either the consensus costs or
group cohesion costs differ between populations, and the
degree to which decisions are shared or unshared can be
approximated. The Trinidadian guppy (Poecilia reticulata)
offers one such system. Populations of guppies in the Northern
Mountain range of Trinidad have been exposed to either
relatively high or relatively low levels of predation over
both their evolutionary and ontogenetic histories [9,10].
Because group cohesion significantly reduces predation risk
[11,12], this system offers an opportunity to assess whether
group decision-making appears more or less shared between
group members in populations where the costs of group
fragmentation differ. Here, we give groups of guppies a clas-
sic decision-making paradigm [13,14], where groups choose
to swim down one of two arms of a Y-maze. We tested mul-
tiple group sizes to assess whether the patterns observed
were robust to differences in group size. Because positions
at the front of groups are more conducive of leadership,
and in many animal groups information flows from the
front to the back of groups, [15–17], positional changes
within groups appear to be informative about who is dispro-
portionally influencing the decision-making process [13,18].
We therefore calculated the number of times individuals
switched positions within the group before they reached a
decision, with increased positional switching acting as a
proxy for more distributed decision-making. Furthermore,
using a simple one-dimensional model, we explored how
differences in how individuals moved might result in different
amounts of positional switching within groups.
2. Material and methods
(a) Experimental methods
Adult female guppies (P. reticulata) were caught from four
locations with high predation risk (Arima, Lower Guanapo,
Lower Lopinot and Tacarigua rivers) and four locations with
low predation risk (Paria, Upper Guanapo, Upper Lopinot and
Upper Turure rivers) in July 2013. High predation sites contain
Crenicichla frenata,Hoplias malabaricus or Aequidens pulcher
which prey on adult guppies, whereas these predators are largely
absent from low predation sites, although low predation sites do
contain Rivulus hartii which prey on juvenile guppies [9,18].
Fish were transported back to the University of the West
Indies, St Augustine Campus, where they were housed in
120 cm diameter circular holding pools (approx. 90 fish per
pool) in an outdoor enclosure that was shaded between 08.00
and 14.00 h (when trials were run). Water depth in the pools
was maintained between 10 and 13 cm, and the pools were emp-
tied, rinsed and refilled between stocking fish from different
populations. We suspended a clear polythene sheet over the
housing pools and test arena throughout the study to stop rain
falling in the pools.
For each trial, groups of two, four or eight fish with approxi-
mately the same body length were caught from the housing
pools and placed into a 15 × 15 cm transparent plastic box at
the end of the stem of a Y-maze (stem 15 cm wide, 71 cm long;
figure 1a). Following 2 min of acclimation, the box was remotely
lifted, allowing the shoals to explore the novel maze environ-
ment. Groups swam down the stem of the Y-maze before
deciding to swim into the left or right arm of the maze. Trials
were filmed with a Canon 550D DSLR camera mounted 1.25 m
above the maze at 25 fps and a resolution of 1920 × 1080 pixels.
We tested group sizes of two (n= 77), four (n= 76) or eight
(n= 77) fish, with each group size being tested once in a block
of three trials, and the order of testing randomized within each
block. Fish were never used in more than one trial. We used
automated tracking software [19] to track the positions and
orientations of fish as they made a decision. In particular, we
measured the number of times the group did not reach a consen-
sus (defined when at least two group members chose different
arms of the Y-maze to swim down), the mean speed of fish,
their cohesion (median distance of group members to the
group’s centroid), the number of times they switched position
(see Results) and the number of movement decisions fish made
per second (see Results). All measures were calculated from the
time a fish entered the blue region in figure 1auntil a fish crossed
into one of the arms of the Y-maze (dashed white lines in
figure 1a). Group cohesion was only measured during times
no gravel
gravel
low predation
total number of switches
high predation
80
0
284
group size
20
13
5
4
67
8
240
60
(a)(b)
Figure 1. (a) The experimental Y-maze. Tracking is superimposed on a frame for one of the trials of eight fish. The numbers next to each fish represent their
positional ranks within the group on that frame. The left arm of the Y-maze contained a gravel patch (off-screen), while the right arm contained no patch. This was
designed to create an asymmetric choice. (b) Boxplots of the total number of times individuals switched position in the group. Raw data points are shown as grey
circles. The central line on each box depicts the median, and the top and bottom edges of each box represent the 25th and 75th percentiles. Whiskers extend to
data points not considered outliers.
royalsocietypublishing.org/journal/rsbl Biol. Lett. 15: 20190556
2

when all group members were simultaneously tracked. All
measures were analysed using linear or generalized linear
mixed models (see electronic supplementary material for
further details). All models included predation regime (high
or low), group size and the mean body size of fish (standard
length measured from stills in the videos) in each group
as fixed effects. As expected, fish from high predation popu-
lations were significantly smaller (2.02 ± 0.48 cm, mean ± s.d.)
than fish from low predation populations (2.29 ± 0.36 cm,
mean ± s.d.; linear mixed model, likelihood ratio test (LRT):
28.97, p< 0.001), making body size an important covariate in
our models. Population was included as a random effect in
all models. The significance of each term within the models
was tested using LRTs to compare models with and without
the term of interest. All statistical analyses were carried out in
R v.3.1.2, and data are available in the electronic supplementary
material.
3. Results
The proportion of groups that split apart during the decision-
making process did not differ between the two predation
regimes (LRT = 1.61, p= 0.20; only 33/231 groups split). Fur-
thermore, fish from the different predation regimes did not
differ in their median swim speeds as they made these
decisions (LRT = 0.42, p= 0.52). Groups of fish from high
and low predation environments, therefore, made similarly
fast and cohesive decisions.
We next investigated whether individuals within groups
from different predation regimes contributed to the consensus
decisions more or less equally. To measure this, fish were
ranked from 1 to nas they swam down the stem of the Y-
maze (shaded blue region in figure 1a), with fish at the front
of the group given a ranking of 1 and the fish at the back of
the group, n(figure 1a). We then calculated the number of
times these ranks changed in the times leading up to the final
decision (when the first fish crossed a dashed line in figure 1a).
Note that if a pair of fish switched their positions, this was
counted as two switches, and we controlled for potential differ-
ences in cohesion between the populations by including
cohesion as a covariate in the models. Fish from high predation
environments switched position more often than fish from low
predation environments (LRT = 5.12, p=0.024; figure 1b),
and as expected, larger groups also made more switches than
smaller groups (LRT = 122.8, p<0.001; figure 1b). These effects
were also observed when considering only switches that
occurred at the front position of the group (predation: LRT =
7.07, p< 0.01; group size: LRT = 20.28, p<0.001).
We then investigated the potential mechanism for how
fish from high-predation environments made more switches
in positions than fish from low predation environments. Gup-
pies, as in many other species of fish, move with intermittent
changes in speed, which can be thought of as movement
decisions [20]. We identified the number of movement
decisions that fish made per second by identifying the
times when fish’s speeds were at a minimum (see grey mar-
kers in figure 2a). After controlling for the effects of median
speed (LRT = 197.6, p< 0.001) and body size (LRT = 22.1,
p< 0.001), fish from high predation environments still made
more decisions per second than fish from low predation
environments (LRT = 4.31, p= 0.038; figure 2b).
To test whether differences in the rate at which fish
updated their position could explain differential switching
behaviour between the populations, we built a simple one-
dimensional self-propelled particle model capturing the
dynamics of guppies’movements. On each time step,
agents updated their position along an one-dimensional
world with a probability, p, that was determined by the
mean update frequency of fish in either low ( p= 0.0368) or
high ( p= 0.0463) predation environments (figure 2b). If fish
updated their position, they moved for a uniformly randomly
determined distance in the range, 0–d(where d> 0). The only
social interaction we implemented was an attraction rule to
neighbours behind a focal individual, that is, if the focal indi-
vidual was in front of its closest follower by more than d,it
did not update its position. One hundred simulation runs
were performed for the same relative number of time steps
it took fish to make the decision for each experimental trial
(n= 231 × 100). This simple model captured the switching
rates observed in the experimental trials, with agents with
higher update probabilities switching position more often
than agents with low update probabilities (figure 2c).
120
speed (mm s–1)
decisions per second
no. switches
3.0 low predation simulated low update
simulated high update
high predation
150
0
50
100
0
0.5
1.0
1.5
2.0
2.5
010
248
9876
time (s)
g
roup size 248
g
roup size
54321
20
40
60
80
100
(a)(b)(c)
Figure 2. (a) Example speed profile of a fish as it moved through the Y-maze. Grey markers represent times when the speed profile has local minima, indicating
times immediately before the fish made a decision to move. (b) Boxplot of the number of decisions fish made per second as a function of group size and low (grey)
or high (blue) predation environments. (c) Results of the simulation where each point represents the average switches a group made out of 100 simulation runs.
Simulations were given two update frequencies: low (grey) or high (blue), respectively, matching the update frequency of fish from low or high predation environ-
ments. The central line on each box depicts the median, and the top and bottom edges of each box represent the 25th and 75th percentiles. Whiskers extend to
data points not considered outliers.
royalsocietypublishing.org/journal/rsbl Biol. Lett. 15: 20190556
3

4. Discussion
Groups of fish from high predation environments switched
positions more often, and made more movement decisions
per second, than fish from low predation environments. In
a simple agent-based model, the increased frequency of asyn-
chronous movement decisions was associated with this
increased positional switching. These results are consistent
with theoretical predictions that collective decision-making is
more equally shared between group members in environments
where the costs of group fission are higher [7,8].
Oscillations in speed and switching of positions are
thought to break visual occlusion between group members,
thereby facilitating the more efficient spread of information
through groups [21]. Mechanisms that promote the likelihood
that multiple individuals contribute towards detecting and
sharing information about potential sources of risk, therefore,
might be favoured in environments where those threats are
higher. Indeed, such mechanisms could allow the collective
pooling of information and the emergence of swarm intelli-
gence [22], especially when information collected by group
members is uncorrelated [23,24]. While, in our model,
increased asynchronous movements could explain increased
positional switching, more frequent movements are also
likely to be coupled with increased energetic requirements.
This may explain why increased positional switching may
not be adopted in environments where information sharing
might be less important, such as when predation risk is
relatively lower.
While we interpret our results in the context of decision-
making, it is important to consider other mechanisms that
could contribute towards increased positional switching in
high compared with low predation environments. Higher
sensitivity to risk [25], swimming performance [26] or
trade-offs in occupying rewarding yet risky positions in
groups [12] may contribute towards increased positional
switching in high compared with low predation environ-
ments. While these factors are not mutually exclusive from
more or less distributed decision-making processes, future
work should attempt to control for these factors when inves-
tigating the importance of positional switching during
decision-making. Our work suggests, however, that popu-
lations have intrinsic differences in the degree to which
decision-making is shared between group members, and
this could be ultimately shaped by differences in the ecologi-
cal conditions that these populations experience.
Ethics. All procedures were approved by the University of Bristol
Ethical Review Group (UIN 13/028).
Data accessibility. Data available from the Dryad Digital Repository:
https://doi.org.10.5061/dryad.nvx0k6dn6 [27].
Authors’contributions. J.E.H.-R., A.S.I.W. and C.C.I. contributed to the
conception and design of experiments. A.S.I.W. and C.C.I. contribu-
ted to the acquisition of data. J.E.H.-R., A.S.I.W., I.W.R. and C.C.I.
contributed to the analysis and interpretation of data. All authors
contributed intellectual content to drafting the article and revising
it critically. All authors approved the final version of the manuscript
and agree to be held accountable for the content therein.
Competing interests. The authors declare they have no conflicts of interest.
Funding. This work was supported by the Natural Environment
Research Council grants nos NE/K009370/1 and NE/P012639/1
awarded to C.C.I. and a Swedish Research Council grant no. 2018-
04076 awarded to J.E.H.-R.
Acknowledgements. We thank Kharran Deonarinesingh and Dr Matthew
Edenbrow for support and helpful discussions, and Dr Kurvers and
two anonymous reviewers for their critiques of our work.
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