Ancestral loss of the maxillary sinus in Old World monkeys and independent acquisition in Macaca

Abstract

Cercopithecoid monkeys are unique among primates in that all species (except macaques) lack a maxillary sinus, an unusual condition among eutherian mammals. Although this uncommon distribution of cranial pneumatization was noted previously, the phylogenetic ramifications have not been investigated fully. Recently, character state optimization analysis of computed tomography (CT) data from extant Old World monkeys suggested that the loss of the sinus may have occurred at the origin of the group, unlike previous hypotheses positing only a reduction in size of the structure. To critically evaluate the "early loss" hypothesis, a recently recovered complete cranium of Victoriapithecus macinnesi from Maboko Island, Kenya, was examined by CT to determine the extent of its cranial pneumatization. This taxon is crucial for evaluating character state evolution in Old World monkeys, due to its phylogenetic position, preceding the cercopithecine/colobine split. CT analysis reveals only cancellous bone lateral of the nasal cavity, indicating that Victoriapithecus does not possess a maxillary sinus. Phylogenetic evaluation of the fossil with extant catarrhine taxa strongly supports the early loss of the sinus in cercopithecoids. The results suggest that the maxillary sinus found in the genus Macaca is not homologous with that of other eutherians, which may provide insights into the origin and function (if any) of the paranasal pneumatizations.

Minor contributions of the maxillary sinus to the air-conditioning performance in macaque monkeys

“…The advantages of such a spandrel-like feature are probably varied for different clades. The paranasal sinus is absent from most clades of the Old World monkeys, but the MS re-emerged in the crown lineage of macaques since its ancestral loss from Old World monkeys (Koppe and Ohkawa, 1999;Rae et al, 2002;. Thus, the MS might confer specific functional advantages in macaques.…”

“…MS pneumatization is always found in macaques and sometimes in baboons and gelada (Papio and Theropithecus), whereas it is absent in other extant Old World monkeys (Koppe and Ohkawa, 1999;. This feature is believed to have arisen independently in these lineages as the paranasal sinuses, including the MS, were lost once in a common ancestor of extant Old World monkeys (Rae et al, 2002). The performance of the air conditioning depends mainly on how the air flows through the nasal cavity (Lindemann et al, 2004;Naftali et al, 2005;Kumahata et al, 2010;Hanida et al, 2013).…”

Nasal Anatomy of Paradolichopithecusgansuensis (Early Pleistocene, Longdan, China) with Comments on Phyletic Relationships among the Species of this Genus

“…The findings would demonstrate intrageneric variation in the presence or absence of a maxillary sinus in the extinct genus . However, such a variation has not been reported, so far, in extant catarhines [Koppe and Ohkawa, 1999;Rae et al, 2002;Nishimura et al, 2005;Rossie, 2006]. Thus, the morphological discrepancy could reflect an interge-neric diversification and distinct phyletic affiliations of the Senèze and Kuruksay specimens.…”

“…Recently, Nishimura et al [2007,2009] examined the internal architecture of the Kuruksay and Senèze crania to test this issue. Among cercopithecines, the maxillary sinus within the cranium occurs only in the crown species of macaques and is regarded as a derived feature [Rae et al, 2002;Rae and Koppe, 2004;Rae, 2008]. Both species, in adults, had a nasal cavity expanding laterally to make a thin maxillary body at the anterior level of the cheek teeth.…”

Nasal architecture in <i>Procynocephalus wimani</i> (Early Pleistocene, China) and implications for its phyletic relationship with <i>Paradolichopithecus</i>

“…The maxillary sinus is a paranasal sinus that communicates with the middle meatus of the nasal cavity and pneumatizes the maxilla; this feature is considered to form only in macaques among the extant cercopithecoids including papionins (Koppe and Ohkawa, 1999;Rae et al, 2002;Ito et al, 2009). It is believed that the paranasal sinuses-including the maxillary sinus-were lost in the common ancestor of extant cercopithecoids, and that the maxillary sinus arose again in the crown lineage of macaques (Rae et al, 2002). Thus, such morphological heterogeneities contribute to confusion in arguments about the phylogenetic placement of Procynocephalus and Paradolichopithecus.…”