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EXPLORING THE CONCEPT OF PHENOTYPIC
ACCOMMODATION: THE CASE OF THE LOSS OF AIR SACS
LLUÍS BARCELÓ-COBLIJN*1
*Corresponding Author: lluis.barcelo@uib.cat
1Laboratori d’Investigació en Complexitat i de Lingüística Experimental (LICLE),
Universitat de les Illes Balears, Palma, Spain
During human evolution our ancestors developed a new phenotype that excluded an
organ present in all extant great apes: laryngeal air sacs. This change has been
acknowledged as an important step towards modern human phonetics. However, to date
there is little reflection about how to conceive such a drastic evolutionary change within
the subtribe Hominina. Here we propose the theoretical integration of air sacs loss as a
case of phenotypic accommodation, a notion that helps to understand how our ancestors
managed to survive, accommodating and consolidating the phenotype without air sacs,
paving the way for a new phonetic system.
1. Laryngeal air sacs and Hominoidea
Laryngeal air sacs is a primitive trait present in many mammals: cetaceans like
dolphins and whales, some ungulates (e.g. takins, from the Hymalayas) and also
in many primates. Hewitt et al. (2002) showed that, within 128 primate species,
up to 72 still have this anatomical feature. Schön Ybarra (1995) attested up to
four different kinds of laryngeal air sacs within primates: (1) lateral ventricular,
(2) subhyoid, (3) infraglottal and (4) dorsal. The first one is present in all great
apes with the exception of H. sapiens. Air sacs are present in juvenile apes, even
in fetuses and neonates (Stark & Schneider 1960). Steele et al. (2013) used 3-D
reconstructions and observed that air sacs in chimpanzees are lateral ventricular,
extending in a position behind the clavicle bone.
1.2. Possible functions of air sacs
The relation of the vocal tract and air sacs and their potential functions is
controversial, since their potential functions could be several and not all species
use air sacs for the same functions: for saving exhaled air (Negus, 1949); for the
Barceló-Coblijn, L. (2022). Exploring the Concept of Phenotypic Accommodation: The Case of the Loss of Air
Sacs. In Ravignani, A., Asano, R., Valente, D., Ferretti, F., Hartmann, S., Hayashi, M., Jadoul, Y., Martins, M.,
Oseki, Y., Rodrigues, E. D., Vasileva, O. & Wacewicz, S. (Eds.): Proceedings of the Joint Conference on
Language Evolution (JCoLE). doi:10.17617/2.3398549.
reduction of hyper-ventilation (Hewitt et al., 2002); for generating a new sound
source and stronger and longer lasting calls (Fitch & Hauser, 2003). Lieberman
(2011) notes that air sacs are probably related to vocalization since inspiring
carbon dioxide-rich air is not as useful as controlling speech. Falk (1975)
pointed out that the vertical movement of the hyoid bone also compresses the
orifice of the laryngeal air sacs and hence, participating in the mechanics when
air sacs are emptied out and filled up. De Boer (2008) and Riede et al. (2009)
created several models showing the influence of the sound produced by air sacs
on the sound produced by vocal folds, while experimental research shows that,
when both kind of sounds become superimposed, modern humans have
difficulties in order to distinguish vowels properly (de Boer, 2012). Although
Harrison (1995) dismissed the idea that air sacs are not necessary for
vocalizations, several scholars do not agree. Lieberman (2010: 333) recalls as
well that another function of air sacs in gorillas is acting “like a resonating
drum” when gorillas thump their chest. More recently, Perlman & Salmi (2017)
analyzed the vocalizations of gorillas and suggest that this species could use
them for male display.
1.3. Abrupt change and the view of complexity
During the evolution of the subtribe Hominina, laryngeal air sacs disappeared at
some point. The key feature to discern the presence or absence of air sacs in the
fossil record seems to be the morphology of hyoid bone. The australopithecine
(Au. afarensis) hyoid bone found, by Alemseged et al. (2006) in Dikika
(Ethiopia), shows a primitive morphology that would suggest the connection of
air sacs to the respiratory system and, hence, to the whole apparatus in charge of
speech. The shape of the Dikika hyoid shows a deep bulla, while the shape of
the H. sapiens hyoid describes an arch, without that deep cavity on the body
section. The deep bulla would be a result of the development of the individual,
from the direct contact of the tissues of air sacs to the hyoid bone.
The next fossilized hyoid bone from the fossil record seemed to belong to a
H. erectus (Capasso et al., 2008). That particular hyoid bone showed a modern
morphology, i.e. there is no cavity or bulla shape to which air sacs could be in
contact with. However, a second examination by Capasso et al. (2016)
confirmed that that bone was “too thick and short to be the body of human
hyoid”. Finally, the neanderthal hyoid bone is quite similar to the H. sapiens’
hyoid bone (Arensburg et al., 1989; Bar-Yosef et al., 1992).
Thus, at some temporary point of the early stages of genus Homo –
somewhere between the Australopithecus and H. erectus clades–, an early
hominin started making steps into modern speech. A plausible, falsifiable
hypothesis is that H. habilis could be that hominin. Suggestions about H. habilis
capability for speech are not new at all (Tobias, 1987), but information about
this hominin is still too scarce and contentious (Wood & Collard, 1999) and,
hence, this hypothesis is, for the moment, still more grounded upon plausible
ideas than upon solid data from the fossil record.
1.4. Modularity and complexity
The enigma of air sacs loss in our lineage needs an explanation integrating
the fact that the tissue of an air sac is always in physical contact with other
tissues: hard tissues (the hyoid bone) and soft tissues (muscles and ligaments).
This fact establishes a direct relationship between them, since all tissues interact
with each other, not only due to contact, but also through the movements of the
body (e.g. movements of the laryngeal muscles when producing sounds or
during deglutition; or while turning the head). In fact, this can be considered as a
collection of interacting elements or, in other words, a complex system. In such
systems, the deletion of some well-connected elements leads to a reorganization
of the system.
The structure of organisms seem to present a modular building schema
(Wagner, 1996; Schlosser & Wagner, 2004; Callebaut & Rasskin-Gutman,
2005). Heads have been analyzed as a complex system which integrates several
modules and submodules, which include different sets of bones (more than 20),
teeth (up to 32), a brain, sensory organs, muscles, ligaments, cartilages, veins,
nerves, etc., showing altogether an evident modular organization (Lieberman,
2011: 8-12). Heads include the neck and all its hard and soft tissues. Inside the
human neck two passages can be detected, one for the air and another for the
food. Anatomical network analyses have revealed musculoskeletal modularity in
primates (Esteve-Altava et al., 2015a; Esteve-Altava et al., 2015b; Powell et al.,
2018).
In a recent network analysis of musculoskeletal organization, Powell et al.
(2018) show that, in spite of having more musculoskeletal elements (up to 157),
humans do not seem to be more complex than other great apes. These authors
argue that “even major changes in function […] can occur without profound
changes to the network organization and modularity of the whole system”.
Although Powell and collaborators include only direct musculoskeletal
connections and not organs like air sacs, this reflection is still valid for the
discussion on the evolution of air sacs: air sacs can disappear, as it has occurred
in many taxa, without compromising the network organization, but affecting the
function of the module. Following Powell et al. (2018), developmental plasticity
can facilitate the accommodation of functional and anatomical modifications
without conditioning severely the network configuration.
Being it as it may, when an individual develops following a divergent and
atypical developmental path, for example lacking (part of) an organ, the
unexpected phenotype can provoke that other tissues of the system develop
abnormally as well, due to the absence of physical opposition, and due to the
“departure” –metaphorically speaking– from what was “planned” by the
original, species-specific, body schema. Hence, soft tissues interact with hard
tissues through physical contact. Lieberman recalls a good example of it in
humans: an infant born lacking eyes will probably develop “tiny orbits with
abnormally small upper faces because the eyeball normally pushes out the bones
that form the orbital cavity walls” (2011: 53). Similarly, the air sacs loss had to
have consequences for the surrounding tissues.
Other forces, like persistent muscular movements, if lasted through
generations, could also exert an influence on the phenotypes, which could have
been finally selected. Far from simply resorting to Lamarck’s (1809) Zoological
Philosophy, we advocate a hypothesis in which phenotypes, not mutations, are
the selected ones (West-Eberhard, 2003). For example, recent analyses of dry
skulls of both humans and chimpanzees suggest a link between the large number
of mandibular movements of muscles involved in speech (much larger than
those used in chewing) and the morphology of the mandibular space in relation
to the tongue (Bermejo-Fenoll et al. 2019). In spite of the difficulty for showing
a cause-effect relationship, Bermejo-Fenoll and colleagues could show that H.
sapiens’ ancestors followed an evolutionary trend which, progressively and
increasingly, included more and more movements that today are related to
modern speech, like for example lip smacking and oscillatory movements of the
jaw (Ghanzafar et al., 2013; Ghanzafar et al., 2012; MacNeilage & Davis, 2005).
Anyway, it seems out of question that, at some point between australopithecines
and modern humans and –we suggest– after the disappearance of air sacs, the
physical context of speech and the laryngeal structure changed, paving the way
to new motor routines which could involve more (and perhaps new) movements
that today are related to modern speech.
2. Air sacs loss as a case of phenotypic accommodation
West-Eberhard (2005a: 6547) recalls that “frequency of expression does not
depend on the frequency of the inducer (mutation or environmental factor)
alone”. Thus, according to West-Eberhard’s (2003, 2005b) proposal,
evolutionary selection combines both natural and sexual or social selection, and
hence, genes would be followers, not leaders in adaptive evolution. We think
this is a good theoretical framework for a change like the loss of air sacs. This is
something that has not been yet approached and, thus, there are some
possibilities open to inquiry. One possibility is that the first individuals lacking
air sacs represented atypical phenotypes within their group of conspecifics.
Hence, it is expectable that the disappearance of air sacs from the body schema
altered, even if slightly, some developmental patterns during ontogeny, and thus
yielding new, different phenotypes in adult individuals. Some available evidence
from comparative studies do support such a view: works on the ontogeny of the
descent of the hyolaryngeal complex and the root of the tongue takes place at
about 3 months of age (Lieberman et al., 2001). By contrast, at 4 months of age
the initial pouch that will become the air sac is already visible in chimps
(Nishimura et al., 2007).
The observable fact is that this new phenotype somehow reached
stabilization, and one of the reasons could be that it was not incompatible with
survival. This can be interpreted as an indication (though still not confirmed
evidence) of a fitness effect. According to West-Eberhard (2005a), if the new
phenotype has a fitness effect, then selection occurs. Were this the case of air
sacs loss, it could be conceived as a phenotype that has been consolidated,
becoming the typical phenotype of current H. sapiens. Observed through this
lens, thus, the air sacs loss could be classified a case of phenotypic
accommodation (West-Eberhard, 2003; 2005b). Phenotypic accommodation
takes place when an individual develops plastically, adapting the organism to
new environmental inputs (here “environmental” refers to all levels in biology,
from cells to ecological niches). If the new inputs persist and other conspecifics
can develop the same adaptive phenotype as well, this new phenotype could
become stabilized by, for example, new mutations promoting and reinforcing it.
Arguments supporting this hypothesis are, for example, that air sac loss is a
consolidated phenotype in many primate species, some of them phylogenetically
distant from one another (cf. Hewitt et al., 2002). Thus, it seems to be a
recurrent homoplasy within the Primates order. Recurrent phenotypes with
discontinuous phylogenetic distributions have been detected in many taxa (cf.
West-Eberhard, 2003, for a highly detailed revision). Moreover, the existence of
both phenotypes within Primates suggests ancestral developmental plasticity for
producing both forms (West-Eberhard, 2005b: 6546). Were the air sacs loss
phenotype dependent of a mutation (or methylation) only, it would be a
mutation/methylation that has appeared many times and hence, less plausible.
Thus, phenotypic plasticity seems to be a good candidate for the origins of air
sac loss, given the fact that it can account for the repetition of homoplasies in
different primates and in different stages of phylogeny. Moreover, phenotypic
accommodation could give time to this developmental variant for becoming
stabilized within populations and species. The absence of air sacs would have
led the possibility for some individuals to develop towards new phenotypes that
were compatible with life (here we follow Pere Alberch’s (1989) “logic of
monsters” and assume the idea of a phenotypic space of biological possibilities).
Let us remark that this hypothesis is conceived as a phenotypic possibility for
some ancestors of H. sapiens, and not for all species that have evolved towards
phenotypes lacking air sacs. The reason is that, usually, there is not a unique
factor affecting the several environmental levels by which an organism is
affected, and each species is affected by a different set of environmental factors
(admittedly, partially coincidental with other species). The first individuals who
developed like that, were at first unusual and atypical. However, some of their
descendants managed to survive, consolidating (accommodating) a phenotype
without air sacs, and thus paving the way for a new phonetic system.
Conclusion
Laryngeal air sacs is an ancestral trait in Primates, while its absence is a
derived characteristic. Both possibilities exist in monkeys, lesser apes
(Hylobatidae) and great apes (Hominidae). It is well-known that the descent of
larynx does not guarantee vocalization (Fitch 2009). Similarly, the lack of air
sacs does not guarantee neither the descent of larynx nor modern speech. But it
was a necessary step for evolving towards what is known today as modern
human speech. Nonetheless, both phenotypes are recurrent and it is puzzling
how to integrate this into evolutionary theory. We propose that this could be a
case of phenotypic plasticity and, more concretely, a case of phenotypic
accommodation. This concept satisfies the recurrence of both phenotypes and
the differences in ontogeny in juvenile chimps and humans. Finally, the concept
of phenotypic accommodation solves the difficulty of linking this evolutionary
change to mutation only, and gives the time a species needs until the new variant
becomes stabilized.
Acknowledgements
This research was partially supported by grant number PID2021-128404NA-I00
from the Ministerio de Ciencia e Innovación (Spain).
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