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A novel obligate cultivation mutualism between damselfish and Polysiphonia algae

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In cultivation mutualisms, farming animals prepare fields for cultivars, enhance their growth and harvest them. For example, in terrestrial ecosystems, plant-herbivore cultivation mutualisms arose between humans and their crops only relatively recently. We discovered an obligate cultivation mutualism between a damselfish and an alga in a coral reef ecosystem. The damselfish, Stegastes nigricans, manages algal farms through territorial defence against the invading grazers and through weeding of unpalatable algae. As a result, the algal farms of S. nigricans are dominated by one species, Polysiphonia sp. We performed an exhaustive survey of algal assemblages inside and outside the territories of five damselfish species around the Ryukyu Islands, Japan, using molecular and morphological characteristics. Polysiphonia sp. 1 grew exclusively inside the farms of S. nigricans, and never elsewhere. Since only Polysiphonia sp. 1 is harvested and consumed by the damselfish as a staple food, this interdependent relationship is an obligate cultivation mutualism. This is the first record of an obligate plant-herbivore cultivation mutualism in a marine ecosystem. Our data also suggest that three other Polysiphonia species are facultatively mutual with, commensal with, or parasitic on other damselfish species.
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Biol. Lett. (2006) 2, 593–596
doi:10.1098/rsbl.2006.0528
Published online 7 August 2006
A novel obligate cultivation
mutualism between
damselfish and
Polysiphonia algae
Hiroki Hata
,
*
and Makoto Kato
Graduate School of Human and Environmental Studies, Kyoto
University, Yoshida-Nihonmatsu, Sakyo, Kyoto 606-8501, Japan
*Author for correspondence (hata@d01.mbox.media.kyoto-u.ac.jp).
Present address: Graduate School of Science, Kyoto University,
Kitashirakawa-Oiwake, Sakyo, Kyoto 606-8502, Japan.
In cultivation mutualisms, farming animals pre-
pare fields for cultivars, enhance their growth
and harvest them. For example, in terrestrial
ecosystems, plant–herbivore cultivation mutual-
isms arose between humans and their crops only
relatively recently. We discovered an obligate
cultivation mutualism between a dam selfish and
an alga in a coral reef ecosyst em. The damsel-
fish, Stegastes nigricans, manages algal farms
through territorial defence against the invading
grazers a nd through weeding of unpalatable
algae. As a result, the algal farms of S. nigricans
are dominated by one species, Polysiphonia sp.
We pe rformed an exhaustive survey of algal
assemblages inside and outside the territor ies of
five damselfish species around the Ryukyu
Islands, Japan, using molecular and mor pho-
logical characteristics. Polysiphonia sp. 1 grew
exclusively inside the farms of S. nigricans, and
never elsewhere. Since only Polysiphonia sp. 1 is
harvested and consumed by the damselfish as a
staple food, this interdependent relationship is
an obligate cultivation mutualism. This is the
first record of an obligate plan t–herbivore culti-
vation mutualism in a marine ecosystem. Our
data also suggest that three other Polysiphonia
species are facultatively mutual with, commen-
sal with, or parasitic on other damselfish
species.
Keywords: obligate cultivation mutualism;
territorial damselfish; Polysiphonia algae; coral reef
1. INTRODUCTION
Cultivation mutualisms between humans and their
crops have evolved through ‘proto-domestication’ in
which humans use and select plants intruding on
human-disturbed habitats (Rindos 1984). In marine
ecosystems, some herbivorous damselfishes and lim-
pets maintain proto-domesticated algal assemblages
(i.e. algal farms) by excluding grazers and cultivating
distinct crop assemblages (Branch 1981; Ceccarelli
et al. 2001). Some limpets on intertidal rocky shores
in South Africa and the west coast of North
America have evolved facultative cultivation mutual-
isms with species-specific but ubiquitous algae
(Branch 1981). Similarly, the damselfish Stegastes
nigricans has been shown to maintain a monoculture
of a lamentous red-alga, Polysiphonia sp., by
excluding invading herbivores (Hata & Kato 2004).
In addition, they remove less-digestible competitive
algae from their algal farms (Hata & Kato 2002).
This intensive management by S. nigricans results in
selection for fast-growing palatable algae. Cage
experiments that exclude a territory-holding damsel-
fish as well as all herbivores have shown that in the
absence of weeding by the fish, the Polysiphonia sp.
are overgrown by other algal species within a week
(Hata & Kato 2003). When only S. nigricans was
removed, its algal farm was invaded by grazers and
denuded of algae in a few days. Thus, intensive
management and aggressive territorial defence allow
the fish to maintain a monoculture of Polysiphonia
sp. on which it feeds as staple food (Hata & Kato
2002). We investigated whether the dependence of
this alga on the fish is obligatory by determining the
occurrence of the alga outside S. nigricans algal
farms. In addition, we investigated whether other
Polysiphonia spp. algae have species-specific relation-
ships with damselfishes and assessed the phyloge-
netic relationships among Polysiphonia spp. algae
that are cultivated by damselfish.
2. MATERIAL AND METHODS
(a) Sampling
We collected Polysiphonia spp. algae and related algal species from
inside and outside the territories of various damselfish. Whether a
site was inside or outside the territories of damselfish was
determined after 20 min of observation immediately before
sampling. To collect algae exhaustively from outside the territories
of fish, we set line transects from the beach to offshore areas,
perpendicular to the shoreline, at two, four and ten reef flats around
Okinawa Island (268 04–52
0
N and 127838
0
–128819
0
E), Ishigaki
Island (248 19–36
0
N and 1248 04–20
0
E) and Iriomote Island
(24815–25
0
N and 123840–55
0
E) respectively, in 2003 and 2004.
The average length of the 16 line transects was 477 m (1057 m
maximum and 156 m minimum). We set a 1!1 m quadrat outside
the territories at 50 m intervals on each transect and scraped all
algae and seagrass inside the quadrat into a mesh bag by grazing
the entire substratum with a knife. In total, 158 samples were
collected from outside damselfish territories. Five territorial herbi-
vorous damselfishes inhabited these study areas: S. nig ricans,
Stegastes lividus, Hemiglyphidodon plagiometopon, Dischistodus prosopo-
taenia and Plectroglyphidodon lacrymatus. Whenever we found these
damselfishes along the line transects, we collected all the algae from
7!7 cm quadrats placed inside the territories. Stegastes nigricans
was found on 14 lines, together with all the other damselfishes
except H. plagiometopon, which was the sole inhabitant of one site
near a river mouth. In total, 53, 18, 9, 19 and 13 samples were
collected from the territories of S. nig r icans, S. lividus,
H. plagiometopon, D. prosopotaenia and P. lacrymatus, respectively.
We also collected algae outside the damselfish territories in
Makaha Beach and Pokay Bay around Oahu Island (21815–42
0
N
and 157838
0
–158816
0
W) in Hawaii in October 2003, and inside
and outside territories of H. plagiometopon in a coral reef around
Koh Hae Island (7846
0
N, and 98821
0
E) in Thailand in March
2004. The algal samples were immediately preserved in 100%
ethanol. In the laboratory, samples were displaced using distilled
water, and all Polysiphonia algae were sorted under a microscope.
Small thalli of Polysiphonia algae collected from inside (nZ67) and
outside (nZ28) territories were classified into 16 species using
molecular data. The total biomass of algae in samples collected
from damselfish territories and that of Polysiphonia species were
measured in wet weight.
(b) Molecular methods
We extracted total DNA from field-collected, ethanol-preserved
algae. A fragment of the 18S ribosomal RNA gene was amplified by
PCR using the primers 5
0
-ACCTGGTTGATCCTGCCAG-3
0
and
G07 and was directly sequenced using the above two and other
four primers (Saunders & Kraft 1994). All the sequences were
deposited in the NCBI GenBank database (accession nos.
AB219858–AB219930).
(c) Phylogenetic analyses
Maximum-parsimony (MP) and maximum-likelihood (ML)
analyses were conducted using PAUP
v. 4.0b10; Bayesian
Received 13 July 2006
Accepted 15 July 2006
593 q 2006 The Royal Society
inference (BI) was conducted using MRBAYES v. 3.0b4. The MP
analyses employed the heuristic search option with TBR (tree
bisection and reconnection) branch swapping and 1000 random-
taxon-addition replicates, identifying the 60 most parsimonious
trees of length 468 steps, C.I.Z0.607 and R.I.Z0.804. Heuristic
MP bootstrap analysis consisted of 1000 pseudoreplicates with 10
random-taxon-addition replicates per pseudoreplicate. The
likelihood ratio test implemented in M
ODELTEST v. 3.06 found that
the TrNCGCI model best fits the sequence data, and this model
was employed in a heuristic ML analysis. A heuristic search with
10 random-taxon-addition sequences and TBR branch swapping
was performed. BI was carried out based on the model of GTRC
GCI with 1 000 000 generations, sampling every 100 generations.
The first 100 samples were discarded as burn-in.
3. RESULTS AND DISCUSSION
Our field collections revealed four Pol ysiphonia,
specialized to specific damselfish species (figure 1;
Fisher’s exact test, all p!0.001; figure 2). These four
Polysiphonia species were morphologically distin-
guished from 21 species known from Japan (Yoshida
1998) in having four pericentral cells, ecorticated
fronds and rarely branched erect axes (figure 1). This
indicates that these Polysiphonia species have never
been found as free-living forms, and thus, we called
the algal species, Polysiphonia spp. 1–4. Polysiphonia
sp. 1, which was always dominant in the algal farms
of S. nigricans, was encountered only inside the farms
of S. nigricans and never outside them, irrespective of
intense sampling (figure 1). This suggests that only
S. nigricans can provide Polysiphonia sp. 1 with the
exposed sunny habitat, where grazing pressure is
moderate and competitive algae are weeded out. In
this way, Polysiphonia sp. 1 is obligately dependent on
S. nigricans. The damselfish manages its algal farm
dominated by Polysiphonia sp. 1 and feeds exclusively
in the farm (Hata & Kato 2002, 2004), suggesting
that the fish depends on Polysiphonia sp. 1 for staple
food. Therefore, this interdependent relationship
between S. nigricans and Polysiphonia sp. 1 is an
obligate cultivation mutualism (table 1). We found
that another damselfish, H. plagiometopon,hada
‘semicultivated’ (Harris & Hillman 1989) Polysiphonia
species. Algal farms of this fish species were always
dominated by Polysiphonia sp. 3 (figure 1). However,
Polysiphonia sp. 3 also inhabited the algal farms of
other damselfishes and was found to occur outside
damselfish farms. This association represents a facul-
tative cultivation mutualism, in which the fish
depends on the alga, but the alga does not necessarily
depend on the fish (table 1).
Polysiphonia species that correspond to ‘weeds’
(Harlan 1992) in terms of human cultivation were
also encountered. Polysiphonia sp. 2 and 4 were
found inside the algal farms of P. lacrymatus and
D. prosopotaenia, respectively. These algae were rare
outside the territories of damselfish, but did not
dominate the farms (figure 1). These algae are
obligately associated with specific fish, whereas the
fish do not necessarily depend on the algae for staple
food. Damselfishes manage their farms in a range
of intensities (table 1), as both monocultures and
mixed cultures (Hata & Kato 2004). Only in
intensive farming systems, damselfish seem to have
evolved obligate cultivation mutualisms, such as
for S. nigricans. Plectroglyphidodon lacrymatus and
D. prosopotaenia, which maintain mixed-culture farms
by management without weeding, appear to engage
only in facultative cultivation mutualism. Stegastes
lividus did not have any species-specific algae in
its mixed-culture farm. On the other hand, the
0
100
50
(b) S. lividus (n = 18)
0
100
50
0
100
50
0
100
50
(d) H. plagiometopon (n = 9)
(e) D. prosopotaenia (n = 19)
(c) P. lacrymatus (n = 13)
P
olysiphonia
sp.2 (n = 3)
***
P
olysiphonia
sp.1 (n = 53)
***
P
olysiphonia
sp.3 (n = 51)
***
P
olysiphonia
sp.4 (n = 9)
***
0
100
50
0
100
50
( f ) outside fish territories (n = 158)
per cent occurrence of each alga inside and outside damselfish territories (%)
1 mm
(a) S. nigricans (n = 53)
Figure 1. Percent occurrence of four Polysiphonia spp. algae
inside and outside the territories of the damselfishes (a)
Stegastes nig ricans,(b) S. lividus,(c) Plectroglyphidodon
lacryma tus,(d ) Hemiglyphidodon plagiometopon and (e)
Dischistodus prosopotaenia. The probability of occurrence of
each algal species among these sites was analysed using
Fisher’s exact test.

p!0.001.
594 H. Hata & M. Kato Obligate cultivation mutualism
Biol. Lett. (2006)
Polysiphonia species that are found exclusively symbio-
tically with specific damselfishes are not monophyletic
(figure 2), suggesting that the adaptations of these
algae to damselfishes originated independently.
Cultivation mutualisms have also evolved between
fungi and terrestrial invertebrates, i.e. ants, termites
and bark beetles (Vega & Blackwell 2005), and a salt
marsh snail (Littoraria irrorata; Silliman & Newell
2003). However, only high-attine ants, termites and
ambrosia beetles occur in obligate cultivation mutual-
isms with an obligate cultivar (Mueller et al. 2005). In
these obligate mutualisms, most farming insects
transplant inocula of fungi from their natal gardens to
new colonies, and thus cultivars are transmitted
vertically (Mueller et al. 2005). In contrast, the
marine cultivation mutualism is analogous to the
ancestral fungus–termite mutualism in which termites
acquire cultivars horizontally via wind-dispersed
spores from other colonies (Aanen et al. 2002;
Korb & Aanen 2003). In the alga–damselfish
mutualism, algal farms of Polysiphonia sp. 1 are mostly
transmitted by S. nigricans from generation to gener-
ation (Lee & Barlow 2001). When colonizing a new
habitat, S. nigricans may use water-borne spores and/
or fragments of Polysiphonia sp. 1 dispersed from
other algal farms. In fact, some Polysiphonia species
have a high capacity for dispersal by spores (Rindi &
Cinelli 2000) or fragments (Eriksson & Johansson
2005), and inside algal farms, both sexual and asexual
spores of Polysiphonia sp. 1 were observed. Addition-
ally, inside artificial cages that excluded all herbivores,
Polysiphonia sp. 1 newly colonized even outside
S. nigricans territories, although they were soon over-
grown by competitive macroalgae. This experiment
showed a high supply of recruits of Polysiphonia sp. 1
in reefs inhabited by S. nigricans (Hata & Kato 2003).
In the terrestrial cultivation mutualisms mentioned
earlier, farming insects harvest decomposition
products that originate from plant remains. In the
damselfish–Polysiphonia cultivation mutualism,
*Snig Ryukyu (6)
*Snig Ryukyu (6)
P. pacifica
Plac Ryukyu (1)
out Ryukyu (1)
P. howei
*
Hpla Ryukyu (1)
*Hpla Thailand (2)
Snig Ryukyu (6)
Sliv Ryukyu (1)
Plac Ryukyu (1)
out Ryukyu (4)
out Hawaii (2)
Womersleyella setacea
100/100
100/100
83/100
64/84
97/100
88/60
P. senticulosa
P. stricta
P. morrowii
out Hawaii (1)
Dpro Ryukyu (3)
other Polysiphonia
Murrayella periclados
Laurencia filiformis
0.005 substitutions/site
51/52
99/98
98/100
Stegastes lividus (Sliv)
Dischistodus prosopotaenia (Dpro)
Stegastes nigricans (Snig)
Plectroglyphidodon lacrymatus (Plac)
Hemiglyphidodon plagiometopon (Hpla)
outside fish territory (out)
Polysiphonia sp.1
Polysiphonia sp.2
Polysiphonia sp.3
Polysiphonia sp.4
D. prosopotaenia
H. plagiometopon
P. lacrymatus
S. nigricans
Figure 2. Phylogeny of Polysiphonia spp. algae found inside and outside the territories of the damselfishes Stegastes nigricans,
S. lividus, Plectroglyphidodon lacrymatus, Hemiglyphidodon plagiometopon and Dischistodus prosopotaenia. The association of each
alga is denoted by the abbreviation and colour of its damselfish host species and by collection site. An asterisk denotes the
dominance of the alga in samples (representing more than 50% of the biomass). Numbers in parentheses indicate the
number of DNA samples. Data for unshaded species denote citations from the NCBI GenBank. The tree was obtained
using ML method, with a log-likelihood score of 4971.063. Branches that collapse in MP, ML and/or BI trees are presented
as dotted lines. Nodal support is assessed by bootstrap values of MP and posterior probabilities of BI (above branches,
MP/BI, respectively). Solid and broken arrows indicate obligate and facultative associations, respectively.
Table 1. Algae that inhabited the algal farms of damselfishes and their relationships with damselfishes.
attributes Polysiphonia sp. 1 Polysiphonia sp. 3 Polysiphonia sp. 2 and 4
habitat only algal farms of
S. nigricans
mainly algal farms of
H. plagiometopon
only algal farms of
P. lacrymatus (sp. 2) or
D. prosopotaenia (sp. 4)
dependence of algae on fish obligate facultative obligate
intensity of farming by fish intensive intensive extensive
dependence of fish on algae obligate obligate partial
type of interaction obligate cultivation
mutualism
facultative cultivation
mutualism
commensalism
status of algae cultivated semicultivated weed
Obligate cultivation mutualism H. Hata & M. Kato 595
Biol. Lett. (2006)
however, the damselfishes harvest photosynthate from
algae cultivated on a sunlit substratum. Thus, this is
the second example of an obligate cultivation mutual-
ism between plant and herbivore, preceded by the
crop–human cultivation mutualism, and the first
example in a marine ecosystem.
We thank E. Toby Kiers, Carl Smith and an anonymous
reviewer for helpful comments on the manuscript, and
Atsushi Kawakita and Yudai Okuyama for their help with
molecular experiments. This study is supported by JSPS
Research Fellowships for Young Scientists.
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Supplementary resources (73)

... The circumtropical distribution of damselfishes is centered on marine coral and rocky reef habitats, with a variety of temperate species occurring at up to 50˚North and South latitude. Members of the family are known for intriguing behaviors such as strong territorial aggression and complex farming or gardening behaviors in which dense stands of filamentous algae are tended for food [42]. Damselfishes have been placed in broad ecological-functional categories ("ecotypes") using combinations of traits such as diet (planktivory, herbivory, and omnivory) and primary feeding location in the water column (benthic, pelagic, intermediate) that are useful for exploring the evolution of damselfish ecomorphology [14,15]. ...
... The Cheiloprionini likely evolved farming once with 4 losses, the Pomacentrinae 3 group twice in Hemiglyphidodon and Neoglyphidodon, and up to 6 origins in the Pomacentrinae (or two origins with multiple losses). Cultivating and defending an algal patch has long been recognized as an unusual level of behavioral complexity in fish feeding behavior [42,101,102], the intricacy of which recently increased as it has been shown to include the domestication of mysid shrimps by damselfishes to help fertilize the garden [103]. All damselfish farmers are benthic, yet most benthic feeders are not farmers, and there is no significant character association between farming presence/absence and dietary ecotype across the phylogeny. ...
Article
Full-text available
The damselfishes (family Pomacentridae) inhabit near-shore communities in tropical and temperature oceans as one of the major lineages in coral reef fish assemblages. Our understanding of their evolutionary ecology, morphology and function has often been advanced by increasingly detailed and accurate molecular phylogenies. Here we present the next stage of multi-locus, molecular phylogenetics for the group based on analysis of 12 nuclear and mitochondrial gene sequences from 345 of the 422 damselfishes. The resulting well-resolved phylogeny helps to address several important questions about higher-level damselfish relationships, their evolutionary history and patterns of divergence. A time-calibrated phylogenetic tree yields a root age for the family of 55.5 mya, refines the age of origin for a number of diverse genera, and shows that ecological changes during the Eocene-Oligocene transition provided opportunities for damselfish diversification. We explored the idea that body size extremes have evolved repeatedly among the Pomacentridae, and demonstrate that large and small body sizes have evolved independently at least 40 times and with asymmetric rates of transition among size classes. We tested the hypothesis that transitions among dietary ecotypes (benthic herbivory, pelagic planktivory and intermediate omnivory) are asymmetric, with higher transition rates from intermediate omnivory to either planktivory or herbivory. Using multistate hidden-state speciation and extinction models, we found that both body size and dietary ecotype are significantly associated with patterns of diversification across the damselfishes, and that the highest rates of net diversification are associated with medium body size and pelagic planktivory. We also conclude that the pattern of evolutionary diversification in feeding ecology, with frequent and asymmetrical transitions between feeding ecotypes, is largely restricted to the subfamily Pomacentrinae in the Indo-West Pacific. Trait diversification patterns for damselfishes across a fully resolved phylogeny challenge many recent general conclusions about the evolution of reef fishes.
... The circumtropical distribution of damselfishes is centered on marine coral and rocky reef habitats, with a variety of temperate species occurring at up to 50° North and South latitude. Members of the family are known for intriguing behaviors such as strong territorial aggression, and complex farming or gardening behaviors in which dense stands of filamentous algae are tended for food (41). Damselfishes have been placed in broad ecological-functional categories ("ecotypes") using combinations of traits such as diet (planktivory, herbivory, and omnivory) and primary feeding location in the water column (benthic, pelagic, intermediate) that are useful for exploring the evolution of damselfish ecomorphology (14,15). ...
... Algal farming or gardening behavior is a complex behavioral trait that has evolved multiple times in three main damselfish lineages, occurring in fishes of diverse body sizes but restricted to the shallow benthic habitats where desirable algae grow (Fig. 5). Cultivating and defending an algal patch has long been recognized as an unusual level of behavioral complexity in fish feeding behavior (41,91,92), the intricacy of which recently increased as it has been shown to include the domestication of mysid shrimps by damselfishes to help fertilize the garden (93). The independent origin of this complex behavior up to a dozen times across the tree, associated with intense aggressive territorial defense behavior, and associated each time with the benthic ecotype that shows the lowest diversification rate across the tree, makes this a promising system for study of the factors that accelerate or slow diversification in damselfishes. ...
Preprint
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The damselfishes (family Pomacentridae) inhabit near-shore communities in tropical and temperature oceans as one of the major lineages with ecological and economic importance for coral reef fish assemblages. Our understanding of their evolutionary ecology, morphology and function has often been advanced by increasingly detailed and accurate molecular phylogenies. Here we present the next stage of multi-locus, molecular phylogenetics for the group based on analysis of 12 nuclear and mitochondrial gene sequences from 330 of the 422 damselfish species. The resulting well-resolved phylogeny helps to address several important questions about higher-level damselfish relationships and the monophyly of genera, including Chromis, Chrysiptera, Parma and Stegastes. A time-calibrated phylogenetic tree scaled using fossil data and recent estimated ovalentarian clade ages, yields an older root age for the family (55.3 mya) than previously proposed, refines the age of origin for a number of diverse genera, and shows that ecological changes during the Eocene-Oligocene transition provided opportunities for damselfish diversification. We explored the idea that body size extremes have evolved repeatedly among the Pomacentridae, and demonstrate that large and small body sizes have evolved independently at least 30 times and with asymmetric rates of transition. We tested the hypothesis that transitions among three dietary ecotypes (benthic herbivory, pelagic planktivory and intermediate omnivory) are asymmetric, with higher transition rates from intermediate omnivory to either planktivory or herbivory. Using multistate hidden-state speciation and extinction models, we found that dietary ecotype is significantly associated with patterns of diversification across the damselfishes, and that the highest rates of net diversification are associated with pelagic planktivory. We also conclude that the pattern of evolutionary diversification in feeding ecology, with frequent and asymmetrical transitions between a small number of feeding ecotypes, is largely restricted to the subfamily Pomacentrinae in the Indo-West Pacific.
... Diverse cultivation mutualisms have evolved across the tree of life, for instance in systems involving snails (Silliman & Newell, 2003), crabs (Thurber et al., 2011), amoeba (Brock et al., 2011), fungi (Pion et al., 2013), three-toed sloths (Pauli et al., 2014), and damselfish (Hata & Kato, 2006). In contrast to these cultivation mutualisms, true agriculture is defined by four components, namely habitual planting, cultivation, harvest, and dependence of the farmer on the crop (Mueller et al., 2005). ...
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Farming of fungi by ants, termites, or beetles has led to ecologically successful societies fueled by industrial-scale food production. Another type of obligate insect agriculture in Fiji involves the symbiosis between the ant Philidris nagasau and epiphytes in the genus Squamellaria (Rubiaceae) that the ants fertilize, defend, harvest, and depend on for nesting. All farmed Squamellaria form tubers (domatia) with preformed entrance holes and complex cavity networks occupied by P. nagasau. The inner surface of the domatia consists of smooth-surfaced walls where the ants nest and rear their brood, and warty-surfaced walls where they fertilize their crop by defecation. Here, we use RNA sequencing to identify gene expression patterns associated with the smooth versus warty wall types. Since wall differentiation occurred in the most recent common ancestor of all farmed species of Squamellaria, our study also identifies genetic pathways co-opted following the emergence of agriculture. Warty-surfaced walls show many upregulated genes linked to auxin transport, root development, and nitrogen transport consistent with their root-like function; their defense-related genes are also upregulated, probably to protect these permeable areas from pathogen entry. In smooth-surfaced walls, genes functioning in suberin and wax biosynthesis are upregulated, contributing to the formation of an impermeable ant-nesting area in the domatium. This study throws light on a number of functional characteristics of plant farming by ants and illustrates the power of genomic studies of symbiosis.
... Some ant species can use other insects, such as aphids, as cattle, or cultivate fungi (Mueller et al. 2005). Numerous taxa in fact benefit from actively managing their resources: agriculture is also found in termites, beetles, fishes, nematodes and even microorganisms (Boomsma 2011;Hata and Kato 2006;Thutupalli et al. 2017). ...
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Agriculture - cultivation of plants, algae, fungi and animal herding - is found in numerous taxa such as humans, but also ants, beetles, fishes and even bacteria. Such niche construction behaviours have evolved independently from hunter/predation behaviours, though many species remain primarily predators. We here investigate when such a transition from predation/hunter behaviour to agriculture is favoured. In these systems where a consumer has a positive effect on its resource, we can expect an allocative cost of agriculture for the farmer, hence modifying the selective pressures acting upon it. The management of the resource may have a negative effect on its consumption: for instance, when the consumer defends the resource against other predators (exploitation cost). In other situations, the cost may occur on the foraging of alternative resources, for instance if the consumer spends more time nearby the farmed resource (opportunity cost). Here, we develop a simple three-species model constituted by a farmer species that consumes two resource species, one of them receiving an additional positive effect from the consumer. We consider two trade-off scenarios based on how the cost of agriculture is implemented, either as an exploitation cost or as an opportunity cost. We use an adaptive dynamics approach to study the conditions for the evolution of the investment into agriculture and specialization on the two resources, and consequences on the ecological dynamics of the community. Eco-evolutionary dynamics generate a feedback between the evolution of agriculture and specialization on the helped resource, that can lead to varying selected intensity of agriculture, from generalist strategies with no agriculture, to farmer phenotypes that are entirely specialized on the farmed resource, with possible coexistence between those two extreme strategies.
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Fungus‐growing termites are among the most successful herbivorous animals and improve crop productivity and soil fertility. A range of symbiotic organisms can be found inside their nests. However, interactions of termites with these symbionts are poorly understood. This review provides detailed information on the role of multipartite symbioses (between termitophiles, termites, fungi, and bacteria) in fungus‐growing termites for lignocellulose degradation. The specific functions of each component in the symbiotic system are also discussed. Based on previous studies, we argue that the enzymatic contribution from the host, fungus, and bacteria greatly facilitates the decomposition of complex polysaccharide plant materials. The host‐termitophile interaction protects the termite nest from natural enemies and maintains the stability of the microenvironment inside the colony. This article is protected by copyright. All rights reserved
... In this work, we show that interactions between algae-farming damselfishes (Pomacentridae) and farm-associated mysid shrimps (Mysidae) constitute a domesticator-domesticate relationship, and that this relationship can provide new insights into the process of animal domestication. Numerous coral reef-associated damselfishes engage in territorial farming behaviors 22 , which are characterized by the tending and defense of turf-algae patches (herein 'farms') on which they primarily feed 23 . Reliance on algae varies across species, spanning from facultative to obligate, with highly dependent species aggressively defending their smaller, more specialized farms 24 . ...
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Domesticator-domesticate relationships are specialized mutualisms where one species provides multigenerational support to another in exchange for a resource or service, and through which both partners gain an advantage over individuals outside the relationship. While this ecological innovation has profoundly reshaped the world’s landscapes and bio- diversity, the ecological circumstances that facilitate domestication remain uncertain. Here, we show that longfin damselfish (Stegastes diencaeus) aggressively defend algae farms on which they feed, and this protective refuge selects a domesticator-domesticate relationship with planktonic mysid shrimps (Mysidium integrum). Mysids passively excrete nutrients onto farms, which is associated with enriched algal composition, and damselfish that host mysids exhibit better body condition compared to those without. Our results suggest that the refuge damselfish create as a byproduct of algal tending and the mutual habituation that damselfish and mysids exhibit towards one another were instrumental in subsequent mysid domes- tication. These results are consistent with domestication via the commensal pathway, by which many common examples of animal domestication are hypothesized to have evolved.
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The nature of domestication is often misunderstood. Most definitions of the process are anthropocentric and center on human intentionality, which minimizes the role of unconscious selection and also excludes non-human domesticators. An overarching, biologically grounded definition of domestication is discussed, which emphasizes its core nature as a coevolutionary process that arises from a specialized mutualism, in which one species controls the fitness of another in order to gain resources and/or services. This inclusive definition encompasses both human-associated domestication of crop plants and livestock as well as other non-human domesticators, such as insects. It also calls into question the idea that humans are themselves domesticated, given that evolution of human traits did not arise through the control of fitness by another species.
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Damselfish of the genus Stegastes inhabit territories and cultivate algal gardens on branching corals of the genus Acropora, aggressively protecting their territories from other fish and preventing predation upon corals within the territory. This behaviour has important ecological impacts and could also be useful in reducing predation on outplanted corals during reef restoration efforts. However, the degree of protection from predators may depend on the ability of Stegastes spp. to recolonise outplanted or newly established coral colonies. Protection of bleaching-resilient massive corals within territories may be of particular importance due to the role of these corals in maintaining coral cover following bleaching events. This study examined whether the presence of Stegastes spp. reduces predation on the massive bleaching-resilient coral Porites lutea in the Mauritian lagoon, and whether Stegastes spp. readily colonise outplanted branching coral fragments and provide adjacent massive corals with indirect protection from predation. Predation levels on wild-occurring and outplanted P. lutea within and outside Stegastes spp. territories were measured. In addition, Acropora muricata branches were outplanted adjacent to wild P. lutea colonies outside Stegastes spp. territories, and recolonisation of these outplants by Stegastes spp. and the impacts of recolonisation on predation were monitored. Both wild and outplanted P. lutea colonies within Stegastes spp. territories sustained less predation damage compared to colonies outside territories. Stegastes spp. recolonized outplanted A. muricata colonies within six months of outplanting, and in doing so returned predation protection to adjacent P. lutea colonies. The ability of Stegastes spp. to colonise outplanted corals and provide indirect protection to adjacent massive bleaching-resilient corals may inform coral outplanting efforts in systems where Stegastes spp. are common. Encouraging Stegastes spp. recolonisation may help to reduce predation damage to corals within territories and potentially improve the success of rehabilitation efforts.
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This review evaluates the generalisation that territorial, herbivorous damselfishes (Pomacentridae) have a major influence on the structure of algal, coral, other invertebrate and fish assemblages on coral reefs, Herbivorous damselfishes are a diverse, widespread and abundant component of reef fish assemblages and their territories take up a significant proportion of the shallow reef substratum, There are several mechanisms by which they potentially affect community structure within territories, including both food consumption and potential "fanning" activities, such as "weeding" of undesirable organisms, "killing" coral to grow algae, providing nutrients for algal "crops" and the aggressive "defence" of vital resources. A synthesis of the literature that documents assemblages both inside and outside territories revealed a number of common patterns. Erect filamentous algae often dominate territories, whereas low-lying crustose coralline and prostrate algae characterise adjacent areas. Furthermore, territories consistently support a greater biomass, productivity and species richness of algae than undefended areas. Experimental studies suggest that damselfishes modify regimes of disturbance and succession but the potentially different effects of feeding, farming and territorial exclusion suggest a more complex interaction of processes. There are also substantial differences between defended and undefended areas in coral species composition and densities of small, mobile organisms such as cryptofauna and juvenile fishes, whereas larger herbivorous fishes are excluded from territories. However, the larger-scale effects of these interactions on the ecology of "included" or "excluded" species has yet to be examined. Many of the above generalisations; may be premature as the literature is clearly biased towards a few larger, more aggressive species that maintain conspicuous algal mats. Our review draws attention to the numerically more abundant and less aggressive herbivorous species whose effects appear to be less dramatic. Furthermore, the spatial and temporal variability in the structure of damselfish communities is largely unknown, further restricting our ability to make valid generalisations. While the effects of territoriality have been tested by damselfish removals, more sophisticated experimental work is needed to assess the relative contributions of selective feeding, reduced herbivory, weeding and other farming activities. These mechanisms will be clearer if we have a better understanding of the function of territoriality, the actual benefits of algal turfs to the damselfishes and the separate tasks involved with establishing and maintaining territories.
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Resident herbivorous damselfishes (Pisces: Pomacentridae) exclude other herbivores from their territories and reduce the grazing pressure within these territories. Among the damselfish, Stegastes nigricans is unique in that it manages a virtual monoculture dominated by the erect filamentous rhodophyte Womersleyella setacea, whereas many other herbivorous damselfishes maintain species-rich farms. We observed the behavior of S. nigricans in a lagoon in Okinawa, Japan, and discovered that this species intensively weeded out specific algae. To analyze weeding selectivity, we compared the algae picked up and discarded by S. nigricans to the algal assemblage found inside the territory. To examine the digestibility of each algal species, 10 damselfish were collected, and algae removed from their stomachs were compared with those found in the intestine and faeces. Inside their territories, S. nigricans selectively weeded out indigestible algae. These algae were late-colonizing Species, and the intensive weeding suppressed algal growth beyond early successional stages. Consequently, selective weeding enabled the fish to maintain virtual monocultural farms of a digestible early colonizer, W setacea, inside their territories.
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Distribution and phenology of some filamentous species of Rhodomelaceae in the low littoral and shallow sublittoral zones of an exposed, western Mediterranean rocky shore were studied for 1 year. The spatial distribution of many species shows a pronounced small-scale (metres or tens of metres) variability. Boergeseniella fruticulosa was most abundant in spring and fertile (tetrasporangia only) in spring and summer. Polysiphonia flocculosa was most abundant in spring and summer and reproductive throughout the year. Polysiphonia opaca was most abundant in summer and fertile in spring–summer. Maximal vegetative development and reproduction of Lophosiphonia cristata were observed in summer; conversely, Polysiphonia ceramiaeformis and Polysiphonia subulata were best developed and mostly reproductive in winter and spring. Womersleyella setacea was the least abundant of the studied species and apparently reproduced only by vegetative growth and fragmentation. The reproductive phenology of the species investigated is generally in agreement with reports for other Mediterranean regions. The life history traits of most species are typical of seaweeds in which environmental factors directly govern the onset of the main activities of the organism by meeting the primary physiological needs (‘season responders’).
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Resident herbivorous damselfishes exclude other herbivores from their territories and maintain dense stands of filamentous algae as algal farms. The damselfish Stegastes nigricans occu- pies coral reefs in the Okinawa Islands, southern Japan, and is unique in maintaining monocultural algal farms of the filamentous rhodophyte Polysiphonia sp. One of the mechanisms by which S. nigri- cans maintains these unique algal farms is by selective weeding of indigestible algae. This study tested the hypothesis that, were it not for management by S. nigricans, monocultures would be taken over by algal succession, even without grazing by other herbivores. We set up S. nigricans-exclusion cages inside and grazer-exclusion cages outside the territories of S. nigricans, and monitored algal succession. After exclusion of S. nigricans, the Polysiphonia sp. monoculture deteriorated rapidly and algal biomass decreased simultaneously. Filamentous rhodophytes replaced Polysiphonia sp. within 2 wk, and were in turn displaced by corticated macrophytes and calcareous algae (which are usually selectively weeded by S. nigricans). Monocultures of Polysiphonia sp. did not appear in the grazer- exclusion cages; pioneer Polysiphonia sp. colonized the areas just after caging, but thereafter was replaced by other filamentous rhodophytes, corticated macrophytes, and calcareous algae. Our experiments demonstrated that S. nigricans maintained monocultures and high biomass of palatable pioneer Polysiphonia sp. against algal succession by intensive farm-management, involving selective weeding.