Within their territories, damselfish cultivate particular algae for consumption. A recent study in BMC Evolutionary Biology shows extensive variation among and within fish species in the composition of these algal 'gardens', varying from monocultures to cultures of mixed species, and in the mode of cultivation. This fish-algal agriculture may provide insight into the early stages of domesticatio

Aanen, D.K.

BMC Biology

English

PubMed

Name not available

As you weed, so shall you reap: on the origin of algaculture in damselfish

Duur K Aanen

Springer - Publisher Connector

NARCIS 

Wageningen Yield 

The transition from a hunter-gatherer to an agricultural 
lifestyle has had dramatic consequences for human 
evolution [1]. It paved the way for the advanced division 
of labor, which characterizes modern societies and which 
was a precondition for their rise. With that, agriculture 
ultimately is at the basis of the exponential increase in 
human population size during the last millennium. What 
is usually less well appreciated is that this transition has 
meant an exponential increase in the population size of 
domesticated organisms compared to their free-living 
ancestors. For example, in the Netherlands there is about 
one domesticated pig for each human, so that the 
domesticated animal outnumbers its wild cousin by some 
three orders of magnitude. Agriculture therefore fully 
satisfies the criterion for a mutualism: a mutually 
beneficial interaction between different species.
More traditional forms of agriculture may shed light on 
the first steps to agriculture. Amerindian farmers propa-
gate cassava (Manihot esculenta) clonally by cuttings. 
However, recombined wild seedlings also appear spon-
taneously in fields, and farmers allow them to grow. Later, 
they recruit some large ones for new cuttings, and it has 
been demonstrated that the selected plants are more 
heterozygous. Therefore, the farmers (unconsciously) 
select for increased heterozygosity [2]. This shows that 
domestication is an ongoing process and that domesti-
cated organisms are not immediately reproductively 
isolated from their wild relatives. This has also been 
shown for domestic cattle where introgression of wild Y 
chromosomes -but not of mitochondria - has occurred in 
northern Europe, suggesting continued mating with wild 
bulls after domestication [3]. And on the human side, 
although a transition back to a hunter-gatherer lifestyle 
from an advanced agricultural society now seems hard to 
imagine, there is evidence for a reversal from a primitive 
agricultural to a hunter-gatherer lifestyle [4].
A different approach to studying the first stages of 
agriculture is to look at non-human agricultural mutual-
isms. Well-known examples are found in two groups of 
social insects - termites and ants - which have indepen-
dently domesticated fungi for food [5]. A recent paper by 
Hata et al. [6] in BMC Evolutionary Biology describes 
details of another fascinating agricultural mutualism, this 
time below the sea surface, between damselfish and fila-
mentous algae. On coral reefs, damselfish individually 
defend territories from invading grazers and maintain 
algal turfs, from which they obtain all their food 
(Figure 1). These turfs are a rich food source and highly 
productive. Most species grow their algal crops as mixed 
cultures of mostly Rhodophyta (red algae). The damsel-
fish lack effective enzyme systems or masticatory organs 
to break down cell-wall material, and hence depend on 
easily digestible algae. The algae they use typically are fast 
growers found in the early stages of a succession.
Earlier work by the same group on the damselfish 
species Stegastes nigricans off the coast of Okinawa pre-
fecture in Japan found that it specialized on the 
filamentous red alga Polysiphonia sp. 1, which it culti-
vated in a near monoculture (Figure  2a). The fish weed 
out most of the other, indigestible, algae, chase away 
other herbivores and harvest the alga as their staple food. 
As this species of Polysiphonia is highly susceptible to 
competition from other algal species, its habitat is limited 
to S. nigricans territories. In this way, the fish and the alga 
Abstract
Within their territories, damselfish cultivate particular 
algae for consumption. A recent study in BMC 
Evolutionary Biology shows extensive variation among 
and within fish species in the composition of these 
algal ‘gardens’, varying from monocultures to cultures 
of mixed species, and in the mode of cultivation. This 
fish-algal agriculture may provide insight into the early 
stages of domestication.
As you weed, so shall you reap: on the origin of 
algaculture in damselfish
Duur K Aanen*
See research article http://www.biomedcentral.com/1471-2148/10/185
CO M M E N TA RY  Open Access
*Correspondence: duur.aanen@wur.nl 
Laboratory of Genetics, Wageningen University, PO Box 309, 6700 AH Wageningen, 
The Netherlands
© 2010 Aanen; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons 
Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any 
medium, provided the original work is properly cited.
Aanen BMC Biology 2010, 8:81 
http://www.biomedcentral.com/1741-7007/8/81
have become highly interdependent and approach the 
state of an obligate mutualism.
Algal analysis
Hata et al. [6] have now carried out a comprehensive 
DNA-based analysis of the algal composition of 320 
territories from 18 species of damselfish, collected 
throughout the Indian Ocean and the West Pacific. The 
authors sketch a more complex picture of the mutualism 
between S. nigricans and Polysiphonia sp. 1 than initially 
believed. While S. nigricans populations in Japan do 
indeed maintain an almost exclusive monoculture of this 
species, in other parts of the fish’s distribution most 
territories contain more diverse mixed cultures (Figure 2b). 
This diversity is manifest in two ways. First, in other areas 
Polysiphonia species constitute much less of the total 
algal biomass per territory; second, in most territories, 
more than one Polysiphonia species is found. Consistent 
with earlier studies, S. nigricans still maintains the most 
specific association of all damselfish studied: in all 117 
territories of S. nigricans studied, close relatives of 
Polysiphonia sp. 1 belonging to a single clade were found. 
Almost all the algae from this clade were exclusively 
found in territories of S. nigricans and never outside 
damselfish territories, suggesting that this mutualism is 
obligate for both partners. The 17 other damselfish 
species studied generally cultivate mixed crops of algae, 
do this in a more extensive fashion than S. nigricans, and 
have less specific associations with Polysiphonia algae.
The monoculture found in the earlier studies was 
initially interpreted as support for a more derived state of 
farming in S. nigricans than in other damselfish. Selective 
weeding is unique for S. nigricans: other species also 
chase away competing grazers but they do not weed out 
unpalatable algae [7]. However, the new study shows that 
this intensive agriculture does not lead to a monoculture 
throughout the distribution area of this fish. Variation in 
the intensity of weeding among regions may explain part 
of the variation, but the composition of the local algal 
community might also influence algal composition inside 
the fish territory.
Monoculture versus mixed crop
Theoretical studies have indicated that symbiont related-
ness may be an important stabilizing factor for mutual-
isms (for example, see [8]). The basic idea is as follows. A 
symbiont’s fitness can be partitioned into two compo-
nents: competitive success relative to other symbionts 
associated with the host, and overall success of the group 
of symbionts. As relatedness declines within hosts, a 
symbiont’s success depends more on its competitive 
ability and relatively less on group success. In many cases, 
competitive traits will have negative side effects for the 
host, as symbionts will be selected for fast exploitation of 
the resources provided by the host. Therefore, theory 
suggests that by selecting for competitive traits symbiont 
mixing destabilizes mutualisms.
However, we have to consider the biological idiosyn-
crasies of a particular mutualism to fully appreciate the 
significance of symbiont relatedness. In the damselfish-
alga mutualism, the algae preferred are those that are fast 
growing and do not invest in persistent cell walls. In the 
non-mutualistic situation, these algae are found in the 
early stages of succession. By their continual weeding, S. 
nigricans continuously recreates these early-succession 
conditions. The main determinant of competitive ability 
in these early-succession algae is fast growth. And the 
fast-growing algae are the ones preferred by the fish. 
Therefore, this form of competition increases rather than 
decreases the benefit for the host.
The origin of agriculture
For both humans and non-humans, the transition to 
agriculture was not a conscious decision. Therefore, we 
have to identify the consequences of changes occurring 
in the coevolving organisms that lead to their domesti-
cation [1]. Some plausible scenarios have been sketched 
for domestications by humans. For example, the ears of 
domesticated wheat and barley do not shatter and drop 
their seeds when ripe, whereas those of their wild 
ancestors do, and the seeds are wind dispersed. The non-
shattering trait is caused by a single recessive mutation. It 
seems plausible that humans who collected seeds selected 
the convenient mutant that concentrated the seeds, and 
thus selected (unconsciously) for the non-shattering 
mutation. If some of these seeds were spilled close to 
human settlements, these mutants gained a fitness 
benefit as their seeds could be more effectively dispersed, 
but this depended on intervention by humans [1].
Figure 1. The researcher and the fish. Stegastes nigricans chasing 
Hiroki Hata off its territory in Okinawa, Japan. Photograph kindly 
provided by Hiroki Hata.
Aanen BMC Biology 2010, 8:81 
http://www.biomedcentral.com/1741-7007/8/81
Page 2 of 4
In general, the challenge is to understand the 
counterintuitive combination of being consumed and 
simultaneously gaining fitness. A plausible scenario for 
the origin of termite fungiculture is the initial 
indiscriminate consumption of unspecialized fungi that 
inhabited their nest structure. In all extant fungus-
cultivating termites, the fungus is propagated by the 
consumption of nodules, which contain gut-resistant 
asexual spores, which are mixed with collected plant 
substrate [9]. It seems plausible that the formation of 
asexual spores that could survive gut passage was a key 
innovation in the fungus in response to insect 
consumption. This change turned the disadvantage for 
the fungus of being consumed into a benefit [9]. For other 
insect-fungus mutualisms it has been argued that the 
interaction started with insects acting as a vector for 
fungal dispersal [5].
The ancestors of algacultural fish were omnivorous and 
multiple independent transitions to algaculture have 
occurred (H Hata, personal communication). This is 
consistent with the rather unspecialized nature of this 
domestication. The fish do not plant or inoculate the 
algae, as has been found in older mutualisms between 
fungi and insects [5]. Instead, they remove most of the 
algae from their territories, thereby continuously recreat-
ing the early stages of algal succession. The algae thus 
selected are the algae characterized by fast growth and 
high palatability. It seems plausible that this mutualism 
started by weeding or consumption of all the algae in a 
territory, and that the fast-growing algae remained, and 
started to specialize on this new niche. With their 
behavior, the fish show some parallels with cattle, which 
by grazing create and improve their own niche - grass-
land. The difference is that the fish seem to remove 
unpalatable algae without consuming these, and that they 
are territorial.
Changes in the ‘farmer’
According to the Wikipedia definition of domestication 
(‘the process whereby a population of animals or plants, 
through a process of selection, becomes accustomed to 
human provision and control’), the farmer is the active 
partner and the crop or livestock the passive. However, it 
is increasingly becoming clear that humans themselves 
have also undergone extensive genetic adaptations after 
the adoption of an agricultural lifestyle. For example, the 
persistence of the ability to digest lactose after the 
weaning phase has arisen independently multiple times 
in human populations characterized by a history of cattle 
herding. Likewise, fungus-growing ants have changed 
from carnivorous to vegetarian after the adaption of 
fungiculture. To fulfill the definition of coevolution it 
remains to be shown in which ways the damselfish have 
genetically changed in response to changes in their 
cultivated algae. The recent finding that the gut 
microbiota of Japanese people contains bacteria that aid 
in digesting the seaweed present in sushi [10] nicely 
illustrates the fact that adaptations can occur upon the 
adoption of seaweed in a diet.
Acknowledgements
I thank Fons Debets for useful comments on the manuscript, Thom Kuyper for 
the suggested comparison with grazing cattle, and Hiroki Hata for discussion.
Published: 18 June 2010
References
1. Diamond J: Evolution, consequences and future of plant and animal 
domestication. Nature 2002, 418:700-707.
2. Pujol B, David P, McKey D: Microevolution in agricultural environments: 
how a traditional Amerindian farming practice favours heterozygosity in 
Figure 2. Variations in algaculture by damselfish. (a) A near monoculture of Polysiphonia sp. 1 from a territory of S. nigricans in Okinawa. 
(b) S. nigricans and its more diverse garden off the coast of Kenya. Photographs kindly provided by Hiroki Hata.
Aanen BMC Biology 2010, 8:81 
http://www.biomedcentral.com/1741-7007/8/81
Page 3 of 4
cassava (Manihot esculenta Crantz, Euphorbiaceae). Ecol Lett 2005, 
8:138-147.
3. Gotherstrom A, Anderung C, Hellborg L, Elburg R, Smith C, Bradley DG, 
Ellegren H: Cattle domestication in the Near East was followed by 
hybridization with aurochs bulls in Europe. Proc Biol Sci 2005, 
272:2345-2350.
4. Oota H, Pakendorf B, Weiss G, von Haeseler A, Pookajorn S, Settheetham-
Ishida W, Tiwawech D, Ishida T, Stoneking M: Recent origin and cultural 
reversion of a hunter-gatherer group. PLoS Biol 2005, 3:e71
5. Mueller UG, Gerardo NM, Aanen DK, Six DL, Schultz TR: The evolution of 
agriculture in insects. Annu Rev Ecol Evol Syst 2005, 36:563-595.
6. Hata K, Watanabe K, Kato M: Geographic variation in the damselfish-red 
alga cultivation mutualism in the Indo-West Pacific. BMC Evol Biol 2010, 
10:185
7. Hata H, Kato M: Monoculture and mixed-species algal farms on a coral reef 
are maintained through intensive and extensive management by 
damselfishes. J Exp Mar Biol Ecol 2004, 313:285-296.
8. Frank SA: Host-symbiont conflict over the mixing of symbiotic lineages. 
Proc Biol Sci 1996, 263:339-344.
9. Aanen DK: As you reap, so shall you sow: coupling of inoculating and 
harvesting stabilizes the mutualism between termites and fungi. Biol Lett 
2006, 2:209-212.
10. Hehemann JH, Correc G, Barbeyron T, Helbert W, Czjzek M, Michel G: Transfer 
of carbohydrate-active enzymes from marine bacteria to Japanese gut 
microbiota. Nature 2010, 464:908-912.
doi:10.1186/1741-7007-8-81
Cite this article as: Aanen DK: As you weed, so shall you reap: on the origin 
of algaculture in damselfish. BMC Biology 2010, 8:81.
Aanen BMC Biology 2010, 8:81 
http://www.biomedcentral.com/1741-7007/8/81
Page 4 of 4


Evolution, consequences and future of plant and animal domestication. Nature

Microevolution in agricultural environments: how a traditional Amerindian farming practice favours heterozygosity in

Abstract Within their territories, damselfish cultivate particular algae for consumption. A recent study in BMC Evolutionary Biology shows extensive variation among and within fish species in the composition of these algal 'gardens', varying from monocultures to cultures of mixed species, and in the mode of cultivation. This fish-algal agriculture may provide insight into the early stages of domestication. See research article http://www.biomedcentral.com/1471-2148/10/185</p

Aanen Duur K

Directory of Open Access Journals

As you weed, so shall you reap: on the origin of algaculture in damselfish

Abstract

Similar works

Full text

Available Versions

Name not available

Springer - Publisher Connector

NARCIS

Wageningen Yield

Springer - Publisher Connector

Directory of Open Access Journals