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A novel obligate cultivation mutualism between damselfish and Polysiphonia algae

The Royal Society
Biology Letters
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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 damselfish and
an alga in a coral reef ecosystem. The damsel-
fish, 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 morpho-
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 plant–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 filamentous 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 (26804–52 0N and 1278380–1288190E), Ishigaki
Island (24819–360N and 124804–200E) and Iriomote Island
(24815–250N and 123840–550E) 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. nigricans,
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. nigr 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 (21815–420N
and 1578380–1588160W) in Hawaii in October 2003, and inside
and outside territories of H. plagiometopon in a coral reef around
Koh Hae Island (78460N, and 98821 0E) 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 50-ACCTGGTTGATCCTGCCAG-30and
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 q2006 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 MODELTEST 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 Polysiphonia,
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. lacr ymatus 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 nigricans,(b)S. lividus,(c)Plectroglyphidodon
lacrymatus,(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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Contributors explore common elements in the evolutionary histories of both human and insect agriculture resulting from convergent evolution. During the past 12,000 years, agriculture originated in humans as many as twenty-three times, and during the past 65 million years, agriculture also originated in nonhuman animals at least twenty times and in insects at least fifteen times. It is much more likely that these independent origins represent similar solutions to the challenge of growing food than that they are due purely to chance. This volume seeks to identify common elements in the evolutionary histories of both human and insect agriculture that are the results of convergent evolution. The goal is to create a new, synthetic field that characterizes, quantifies, and empirically documents the evolutionary and ecological mechanisms that drive both human and nonhuman agriculture. The contributors report on the results of quantitative analyses comparing human and nonhuman agriculture; discuss evolutionary conflicts of interest between and among farmers and cultivars and how they interfere with efficiencies of agricultural symbiosis; describe in detail agriculture in termites, ambrosia beetles, and ants; and consider patterns of evolutionary convergence in different aspects of agriculture, comparing fungal parasites of ant agriculture with fungal parasites of human agriculture, analyzing the effects of agriculture on human anatomy, and tracing the similarities and differences between the evolution of agriculture in humans and in a single, relatively well-studied insect group, fungus-farming ants. Contributors Duur K. Aanen, Niels P. R. Anten, Peter H. W. Biedermann, Jacobus J. Boomsma, Laura T. Buck, Guillaume Chomicki, Tim Denham, R. Ford Denison, Dorian Q. Fuller, Richard Gawne, Nicole M. Gerardo, Thomas C. Harrington, Ana Ješovnik, Judith Korb, Chase G. Mayers, George R. McGhee, Kenneth Z. McKenna, Lumila P. Menéndez, Peter N. Peregrine, Ted R. Schultz
... Diverse forms of cultivation have evolved across the tree of life in systems as varied as the cultivation of bacteria by crabs (Thurber et al. 2011), amoebae (Brock et al. 2011), and fungi (Pion et al. 2013; the cultivation of algae by three-toed sloths (Pauli et al. 2014) and damselfish (Hata and Kato 2006); and the cultivation of fungi by snails (Silliman and Newell 2003). In contrast to these cultivation mutualisms, which can involve some form of planting or cultivation such as weeding and harvesting of "crops," true agriculture involves a unique set of behaviors and traits that occur sequentially in which a "farmer" farms a "crop" species. ...
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Full-text available
Contributors explore common elements in the evolutionary histories of both human and insect agriculture resulting from convergent evolution. During the past 12,000 years, agriculture originated in humans as many as twenty-three times, and during the past 65 million years, agriculture also originated in nonhuman animals at least twenty times and in insects at least fifteen times. It is much more likely that these independent origins represent similar solutions to the challenge of growing food than that they are due purely to chance. This volume seeks to identify common elements in the evolutionary histories of both human and insect agriculture that are the results of convergent evolution. The goal is to create a new, synthetic field that characterizes, quantifies, and empirically documents the evolutionary and ecological mechanisms that drive both human and nonhuman agriculture. The contributors report on the results of quantitative analyses comparing human and nonhuman agriculture; discuss evolutionary conflicts of interest between and among farmers and cultivars and how they interfere with efficiencies of agricultural symbiosis; describe in detail agriculture in termites, ambrosia beetles, and ants; and consider patterns of evolutionary convergence in different aspects of agriculture, comparing fungal parasites of ant agriculture with fungal parasites of human agriculture, analyzing the effects of agriculture on human anatomy, and tracing the similarities and differences between the evolution of agriculture in humans and in a single, relatively well-studied insect group, fungus-farming ants. Contributors Duur K. Aanen, Niels P. R. Anten, Peter H. W. Biedermann, Jacobus J. Boomsma, Laura T. Buck, Guillaume Chomicki, Tim Denham, R. Ford Denison, Dorian Q. Fuller, Richard Gawne, Nicole M. Gerardo, Thomas C. Harrington, Ana Ješovnik, Judith Korb, Chase G. Mayers, George R. McGhee, Kenneth Z. McKenna, Lumila P. Menéndez, Peter N. Peregrine, Ted R. Schultz
... In addition, some animals farm all of their food items, be it algae by damselfish ( Lassuy 1980 , Hixon andBrostoff 1983 ) or fungi by leafcutter ants and termites ( Weber 1972, Mueller et al. 2005 . Recent research has been focused on the nutritional exchanges between insects and their farmed species, particularly between ants and their fungi ( Shik et al. 2021 ) , whereas in damselfishes, there is a digestive basis for weeding and defense of monocultures of one particular algal species: They lack a gizzard and the digestive enzymes needed to digest most algae, except the edible species they farm and rarely found outside their gardens ( Hata and Kato 2006 ) . It is hard to imagine taste does not also play some role. ...
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There may be no such thing as a free meal, but many species have evolved mechanisms for other species to consume the literal fruits of their labors. In the present article, inspired by a chef's recognition that such species are “nature's chefs,” we consider food-making species from the plant, animal, and fungal kingdoms, which produce food or mimic food to increase their own fitness. We identify three ways that species can produce or prepare meals—as food, drinks, or lures—and further distinguish between those providing an honest meal and those deceiving consumers with food mimics. By considering these species holistically, we highlight new hypotheses about the ecology and evolution of the widespread phenomenon of organisms that produce food for other organisms. We find surprising and useful generalities and exceptions among species as different as apple trees and anglerfish by examining species interactions across taxa, systems, and disciplines.
... Mutualisms between fungi and fungus-farming insects are model systems for studying co-evolutionary interactions between species (Nygaard et al., 2016;Solomon et al., 2019;Biedermann and Vega, 2020;Pereira and Kjellberg, 2021). Compared to the well-documented fungus-farming mutualisms in some social insects, fungus farming by non-social organisms is uncommon, but includes some examples such as a lizard beetle Doubledaya bucculenta (Toki et al., 2012), weevils in the genus Euops (Coleoptera: Attelabidae) (Sawada and Morimoto, 1986;Kobayashi et al., 2008;Li et al., 2012), a marine snail (Silliman and Newell, 2003), and several species of damselfish (Hata and Kato, 2006). The biological and molecular aspects of fungus-farming mutualisms in solitary, non-social insects have been poorly explored. ...
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Fungus-farming mutualisms are models for studying co-evolutionary among species. Compared to well-documented fungus-farming in social insects, the molecular aspects of fungus-farming mutualisms in nonsocial insects have been poorly explored. Euops chinensis is a solitary leaf-rolling weevil feeding on Japanese knotweed (Fallopia japonica). This pest has evolved a special proto-farming bipartite mutualism with the fungus Penicillium herquei, which provide nutrition and defensive protection for the E. chinensis larvae. Here, the genome of P. herquei was sequenced, and the structure and specific gene categories in the P. herquei genome were then comprehensively compared with the other two well-studied Penicillium species (P. decumbens and P. chrysogenum). The assembled P. herquei genome had a 40.25 Mb genome size with 46.7% GC content. A diverse set of genes associating with carbohydrate-active enzymes, cellulose and hemicellulose degradation, transporter, and terpenoid biosynthesis were detected in the P. herquei genome. Comparative genomics demonstrate that the three Penicillium species show similar metabolic and enzymatic potential, however, P. herquei has more genes associated with plant biomass degradation and defense but less genes associating with virulence pathogenicity. Our results provide molecular evidence for plant substrate breakdown and protective roles of P. herquei in E. chinensis mutualistic system. Large metabolic potential shared by Penicillium species at the genus level may explain why some Penicillium species are recruited by the Euops weevils as crop fungi.
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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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This review provides a brief summary of our field research on the behavioral ecology of coral reef fishes conducted at Sesoko Station, University of the Ryukyus, Okinawa, Japan. We have continued observations and experiments on fish behavior using SCUBA or by snorkeling on the fringing reefs of Sesoko Island since 1982. The results of our four main research subjects, that is, mimicry, parental care and mating systems, bidirectional sex change, and mate choice and alternative mating tactics, all of which have been major subjects of behavioral ecology, are summarized with references and historical information. The titles and speakers of papers, presented at two international meetings organized by the author and held at the Sesoko Station in 1991 and 2004, and field studies conducted on fishes in Sesoko Island by other researchers, including graduate students from various universities, are introduced. The Sesoko Station has been providing excellent facilities for field studies of coral reef fishes and has contributed greatly to the development of the behavioral ecology of fishes.
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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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Insects and fungi have a shared history of association in common habitats where together they endure similar environmental conditions, but only recently have mycologists and entomologists recognized and had the techniques to study the intricacies of some of the associations. This new volume covers “seven wonders of the insect-fungus world” for which exciting new results have become available, often due to the use of new methods that include phylogenetic analysis and development of molecular markers. Eleven chapters of the volume are presented in two sections, “Fungi that act against insects” and “Fungi mutualistic with insects” that cover a number of major themes. Examples of necrotrophic parasites of insects are discussed, not only for biological control potential, but also as organisms with population structure and complex multipartite interactions; a beneficial role for symptomless endophytes in broad-leafed plants is proposed; biotrophic fungal parasites with reduced morphologies are placed among relatives using phylogenetic methods; complex methods of fungal spore dispersal include interactions with one or more arthropods; the farming behavior of New World attine ants is compared with that of humans and the Old World fungus-growing termites; certain mycophagous insects use fungi as a sole nutritional resource; and other insects obtain nutritional supplements from yeasts. Insects involved in fungal associations include--but are not limited to--members of the Coleoptera, Diptera, Homoptera, Hymenoptera, and Isoptera. The fungi involved in interactions with insects may be clustered taxonomically, as is the case for Ascomycetes in the Hypocreales (e.g., Beauveria, Metarhizium, Fusarium), ambrosia fungi in the genera ophiostoma and ceratocystis and their asexual relatives, Laboulbeniomycetes, Saccharomycetes, and the more basal Microsporidia. Other groups, however, have only occasional members (e.g., mushrooms cultivated by attine ants and termites) in such associations. The chapters included in this volume constitute a modern crash course in the study of insect-fungus associations.