Autonomy As A Property That Characterizes Organisms Among Other Multicellular Systems
Autonomy As A Property That Characterizes Organisms Among Other Multicellular Systems
Autonomy As A Property That Characterizes Organisms Among Other Multicellular Systems
ABSTRACT
Biology is full of examples of multicellular (MC) systems which may demonstrate some
organism-like properties but not all of them. Thus, it remains unclear if and when such sys-
tems should be considered as MC organisms, parts of organisms or groups of organisms. We
suggest the notion of autonomy as a possible candidate to ground conceptually MC organisms
and distinguish them from other forms of multicellularity. Considering unicellular systems as
autonomous organisms on the basis of the functional integration required for their metabolic
organization, we argue that MC systems should be also identified as autonomous, but on the
basis of exhibiting a special kind of functionally integrated and differentiated developmental
organization, which unfolds through a self-constructed set of mechanisms regulating the highly
plastic processes that bring about their own constitution as such MC entities.
© Contrastes. Revista Internacional de Filosofía: Suplemento 18 (2013), pp. 357-372. ISSN: 1136-9922
Departamento de Filosofía, Universidad de Málaga, Facultad de Filosofía y Letras
Campus de Teatinos, E-29071 Málaga (España)
358 argyris arnellos, kepa ruiz-mirazo, álvaro moreno
KEYWORDS
AUTONOMY, ORGANISM, MULTICELLULARITY, FUNCTIONAL INTEGRATION,
FUNCTIONAL DIFFERENTIATION, DEVELOPMENTAL CONSTRAINTS, EPIGENE-
TICS, SIGNALING NETWORKS
RESUMEN
La biología está llena de ejemplos de sistemas multicelulares que pueden mostrar algunas pro-
piedades de organismos, pero no todas. De este modo, no está muy claro si estos sistemas deben
ser considerados como organismos multicelulares y cuándo deben serlo. Aquí sugerimos que
la noción de autonomía es un candidato posible para fundamentar conceptualmente los orga-
nismos multicelulares y para distinguirlos de otras formas de multicelularidad. Considerando a
los sistemas unicelulares como organismos autónomos sobre la base de la integración funcional
requerida para su organización metabólica, argüimos que los sistemas multicelulares deben
ser también identificados como autónomos, pero sobre la base de que exhiben un tipo especial
de organización del desarrollo funcionalmente integrada y diferenciada, la cual se despliega a
través de un conjunto auto-construido de mecanismos que regulan los procesos enormemente
plásticos que dan lugar a su propia constitución como tales entidades multicelulares.
PALABRAS CLAVE
AUTONOMÍA, ORGANISMO, MULTICELULARIDAD, INTEGRACIÓN FUNCTIO-
NAL, DIFERENCIACIÓN FUNCTIONAL, CONSTRICCIONES DEL DESARROLLO,
EPIGENÉTICA, REDES DE SEÑALES
I. Introduction
Contemporary attempts to define biological individuality are based either
on physiological and genetic characteristics (see e.g. Santelices 1999), on the
cooperative/competitive behaviors of the entities involved (e.g. West and Kiers
2009; Strassmann and Queller 2010), on evolutionary concepts, like fitness and
adaptation (e.g. Queller and Strassmann 2009; Folse 3rd and Roughgarden 2010)
or on mixed approaches that favor specific aspects of functional integration,
such as germ-soma separation (e.g. Buss, 1987; Maynard Smith and Szathmáry
1995; Michod 2007), resulting in cohesive or policing mechanisms, so that
potential conflict among the constituting units is minimized (e.g. Frank 2003;
Godfrey-Smith 2009).
But each of these aspects does not apply in all cases un-problematically.
For instance, physiological unity is not present in every organism and genetic
relatedness is not strictly necessary for high cooperation, while genetic hetero-
geneity is not always a threat to multicellular integrity (Folse 3rd and Rough-
garden 2010). In many cases potential cooperation does not linearly transform
into actual cooperation, and potential for low conflict does not mean actual
high integration or even actual low conflict (Strassmann and Queller, 2010).
Besides, there are cases of discordant selection, where selection operating at a
lower level may act against the selection at a higher level, even if the alignment
and export of the fitness interests of the component units of an organism could
also result in adaptation at the level of the (multicellular) organism (Gardner
and Grafen 2009; Folse 3rd and Roughgarden 2010). However, adaptation is
not an easy notion to explain, and is often taken to be demonstrated at a given
level of selection, thus resulting in different answers when it is the product of
group selection or of multiple levels of individual selection (Okasha, 2006). In
summary, there is a plurality of views and various difficulties around the pro-
blem of defining the biological individual and there are several criteria, whose
combination generates multiple different verdicts that do not necessarily overlap
and which fail to accommodate many examples we can think of in real biology
(Clarke 2011).
And yet, the clarification of the concept of an ‘individual organism’ is an
important philosophical and scientific problem, not only because the idea of
organism has played a key role in the history of biology (as a central part of
biological explanations ‒i.e., as the locus of mechanisms, of adaptations, of
selective-evolutionary dynamics); but also because, as it is argued in Ruiz-
Mirazo and Moreno (2011), without a strong idea of organism it would be very
difficult to provide a naturalized account of other fundamental concepts like
functionality, agency, autonomy, genetic information, etc.
Accordingly, we believe that a more comprehensive approach to biological
individuality is needed, and we suggest the notion of ‘autonomy’ as a possible
candidate for such an inclusive or comprehensive approach. Autonomy places
the individual organism at the centre of the stage and emphasizes that any
biological individual organism needs to realize the property of maintaining
itself as a metabolic system. Autonomous systems are not independent from
their surrounding, they critically rely on diverse features of the environment
(e.g.: general physico-chemical conditions for viability, energetic and material
availability, etc.) but they continuously generate and regenerate all the constra-
ints and mechanisms upon which the use and management of those resources
is based. Therefore, there is a continuous interplay between the organization of
processes constituting a relatively stable identity (or ‘self’), and the interactions
with the environment that this identity triggers and supports, which are crucial
for its maintenance. So autonomy must be conceived in terms of a particular
connection, or even collaboration with external systems. But, as in the case of
metabolism, it is impossible to talk of autonomy without the specification of
some form of self-constructed, individual identity. On the other hand, biology
shows many collective forms and groupings of entities, which may resemble
several composite forms of autonomy, but it is not clear whether those groupings
should be considered as full-fledged autonomous individuals or as just colonial
systems. Then, assuming that unicellular entities are autonomous organisms, the
question to address would be what sorts of MC systems, if any, meet equivalent
requirements and can therefore be regarded, themselves, as organisms –or, as
higher order autonomous organizations (Ruiz-Mirazo and Moreno 2011).
With this aim, taking into account the main results of current biological
investigations on the developmental processes of different types of MC systems,
we attempt to examine whether the concept of autonomy can account for other
functionally diverse but at the same time integrated forms of collective asso-
ciations of biological entities and processes. In other words, we shall suggest
when and how would it be possible to discern whether a group of cells is just
gathering together temporarily to improve their overall fitness, or irreversibly
becoming part of a higher-order autonomous entity. Certainly, the creation of
a higher order full-fledged autonomous entity requires some kind and degree
of functional integration, as an autonomous system’s creation is not possible
without a stronger subordination of the constitutive elements to the new functio-
nal requirements of the emerging global individual (Ruiz-Mirazo and Moreno
2011). Accordingly, we suggest that with respect to MC collections, autonomy
should be analyzed following at least a set of criteria related to the overall de-
velopmental coordination of the collection, the presence of differentiated cell
types and the regulation of their development, and their respective kind and
degree of functional integration necessary for the development and maintenance
of the organismal level (the level of the whole).
On those lines, in section 2 we discuss that, from an organizational point
of view, MC organisms should be identified by a set of criteria related to the
developmental mechanisms used by the collection of cells to coordinate their
differentiation pathways, in a way that the robust maintenance and potential
reproduction of the whole developing system is ensured through an emergent
functionally integrated organization. In section 3 we examine cases of advanced
bacterial multicellularity and of early eukaryotic multicellularity, where overall
developmental regulation is not that evident and a very limited degree of cellular
differentiation is at place, and we compare them with a case of early metazoans.
In section 4 we argue that although the former cases exhibit substantial coordi-
nation and cohesion (and functional integration surely at other organizational
levels), they do not qualify as autonomous entities, since full-fledged autonomy
at the MC level involves a special kind of regulatory control that provides the
potential for both functional diversification and functional integration required
for the proper and reliable unfolding of a process of development.
1 In N. punctiforme the vegetative cells can also develop into akinetes, spore-like struc-
tures that are more resistant to cold and desiccation conditions, and into hormogonium filaments,
which lack heterocysts, have smaller size and a slow gliding motility, used for short-distance
dispersal. The development of akinetes does not seem to involve any intercellular signaling but
it is strictly triggered by environmental inputs. Hormogonium development will result in one
cell type in the filament and, again, this seems to be triggered by environmental signals followed
by multiple independent (intracellularly controlled) cell divisions for each one of the cells (see
Meeks et al. 2002 for details). It is for those reasons that we do not consider these modalities in
our description of N. punctiforme.
but also the production of PatS. On the contrary, PatS suppresses HetR. In
neighbouring cells, the entry of PatS will prevent the formation of HetR. In
more distant areas, diffusion of PatS may not be sufficient, so new centres of
activation can be formed. 2
A careful analysis of the details of heterocyst development (see e.g. Meeks
et al. 2002; Kumar et al. 2010; Maldener and Muro-Pator 2010) reveals that the
signaling network which guides the development of a differentiating cluster of
cells into one heterocyst at any developmental site in the filament operates un-
der a single constraint (PatS concentration) at the collective level. There seems
to be no generation of other compounds/structures (i.e., no synthesis of any
morphogen or some other kind of signal in the cells where HetR is suppressed
by PatS), which acts intercellularly on the phenotypic traits and organization
of the different cell that produced PatS ‒or on any other neighbouring cell. In
addition to that, heterocysts undergo terminal differentiation, as they lose the
ability to divide. In fact, whether a vegetative cell can be turned into a pro-
heterocyst is strictly connected to its life-cycle stage (Meeks et al. 2002). Now,
this implies a mechanism of differentiation that remains strongly coupled to
the core metabolic requirements of the process of growth and division of the
vegetative cells. In addition, heterocysts development is a terminal event be-
cause they ‘sacrifice’ their ability to reproduce in order to provide surrounding
vegetative cells with combined nitrogen. Moreover, there is a 24h delay in the
growth process of the filament after the development of functional heterocysts,
which is a result of the downregulation of genes related to vegetative growth and
division (Christman et al. 2011). Those two facts indicate that cell division and
cell differentiation cannot be modulated outside of the core metabolic context.
On the contrary, they imply a mechanism of the developmental regulation of
differentiation that remains strongly coupled to the metabolic requirements of
the vegetative cells.
Volvox carteri is a eukaryotic MC system constituted by unicellular algae
and has a developmental process that results in spheroid adults with two cell
types: large reproductive cells (gonidia) and small motile somatic cells. Somatic
cells do not divide but continue beating their flagella, thereby providing the
group with a capacity to swim. The rest of the cells in the group (the germ cells)
divide and produce progeny. Complete germ-soma separation derives from the
fact that, in Volvox carteri, germ cells directly become reproductive gonidia.
A healthy culture of V. carteri will cleave 11 times and will result in di-
vision of labor among (approximately) 2000 somatic cells and 16 germ cells.
During embryogenesis some of the cleavage divisions are asymmetric, produ-
cing large/small sister-cell pairs (Kirk 2005). At the end of embryogenesis the
volume of the gonidial initials is about 30-fold larger than that of the somatic
initials. However, at that stage, cells are only different in size. Then, by a still
unknown mechanism, the size of each sister cell leads to the activation of ei-
ther a somatic or germline program (Kirk 2005). Thus, small cells develop as
biflagellate somatic cells for motility, biosynthesis of the extracellular matrix,
and phototaxis, and large cells develop as non-motile, germ cells specialized
for growth and reproduction.
In the developmental process of V. carteri (see Kirk 1998; 2005 and Hall-
man 2011 for details) the initiation of somatic or gonidial developmental process
is explicitly dependent on the size of each cell and cellular differentiation is
achieved by intracellular cell fate specification. Specifically, V. carteri cells that
are below the threshold diameter of 8 μm at the end of cleavage will activate the
somatic-cell program of differentiation, while cells above that threshold activate
the gonidial program. And this happens even if all of the cytoplasm that they
contain is cytoplasm that would normally have been found in somatic cells. In
addition, the way V. carteri achieves its complete germ-soma separation prohibits
any further flexibility and variability in the genotype-phenotype mapping, as
discussed thoroughly by Nedelcu and Michod (2004). Thus, in V. carteri –even
more explicitly than in N. punctiforme, given the complete germ-soma separation
of the former– cell division remains either totally decoupled (in somatic cells) or
strongly coupled (in germ cells) to cell growth and global system reproduction.
Therefore, we can conclude that the development of cellular differentiation in V.
carteri takes place independently of any constraining signaling structures pro-
duced from other cells in this MC system. Furthermore, as in the N. punctiforme
case, development in V. carteri is also strongly coupled to the core metabolic
requirements of the processes of growth and division, preventing potential me-
chanisms for meta-cellular modulation of the developmental process and the
adaptive evolution of further cell differentiation patterns.
III.2. Developmental regulation in metazoans: the case of a sea urchin
The sea urchin (SU) Strongylocentrotus purpuratus is a small invertebra-
te3 that belongs to the echinoderm phylum. Although it is a relatively simple
most detailed network described in any embryo, which is constantly updated (for more details,
check the website: http://sugp.caltech.edu/endomes/#UpTo30NetworkDiagram).
Acknowledgements
This work has been supported by grants from the Ministerio de Ciencia e
Innovación FFU2009-12895-CO2-02, Ministerio de Economía y Competitivi-
dad FFI2011-25665 and Gobierno Vasco IT 505-10. Argyris Arnellos holds a
Marie Curie Research Fellowship (IEF-273635). Authors would like to thank
also the organizers of the first conference of the AIFIBI (Valencia, Spain, Nov.
2012), where this work was presented, and Antonio Diéguez in particular, for
the opportunity to share these ideas with the Ibero-American community of
philosophers of biology and get insightful feedback from them.
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