Ancestral Loss of Short Wave-Sensitive Cone Visual Pigment in Lorisiform Prosimians, Contrasting with Its Strict Conservation in Other Prosimians

Kawamura, Shoji; Kubotera, Naoya

doi:10.1007/s00239-003-2553-z

Cited by 111 publications

(50 citation statements)

References 38 publications

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“…In the three lorisiform species examined, the S opsin gene has become a pseudogene due to several severe defective mutations (Fig. 3), some of which had been found in two previous studies (18,19). Many of these mutations are shared by the three lorisiform species, indicating that they were acquired in their common ancestor.…”

Section: Resultsmentioning

confidence: 78%

“…Thus, the majority of nocturnal lemuriforms, as well as the two diurnal species sampled, show a functional S opsin gene. For diurnal lemurs, the S opsin- containing cones had previously been detected by electroretinographic flicker photometry (20), and an intact coding sequence of the S opsin has been found (19). What is unexpected is that the majority of nocturnal lemurs examined also have an intact S opsin gene.…”

Section: Resultsmentioning

confidence: 90%

“…The defective mutations found in one tarsier species, the western tarsier, are consistent with the sequence in a study described in ref. 19. In any case, such mutations are probably not incapacitating, because two codons after this original start codon, there is another ATG that can presumably be used as an alternative start.…”

Section: Resultsmentioning

confidence: 99%

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Evidence from opsin genes rejects nocturnality in ancestral primates

Tan

Yoder

Yamashita

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

141

132

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It is firmly believed that ancestral primates were nocturnal, with nocturnality having been maintained in most prosimian lineages. Under this traditional view, the opsin genes in all nocturnal prosimians should have undergone similar degrees of functional relaxation and accumulated similar extents of deleterious mutations. This expectation is rejected by the short-wavelength (S) opsin gene sequences from 14 representative prosimians. We found severe defects of the S opsin gene only in lorisiforms, but no defect in five nocturnal and two diurnal lemur species and only minor defects in two tarsiers and two nocturnal lemurs. Further, the nonsynonymous-to-synonymous rate ratio of the S opsin gene is highest in the lorisiforms and varies among the other prosimian branches, indicating different time periods of functional relaxation among lineages. These observations suggest that the ancestral primates were diurnal or cathemeral and that nocturnality has evolved several times in the prosimians, first in the lorisiforms but much later in other lineages. This view is further supported by the distribution pattern of the middle-wavelength (M) and longwavelength (L) opsin genes among prosimians.T he traditional view of primate evolution (Fig. 1A) holds that the last common ancestor of living primates was nocturnal and that nocturnality has continued uninterrupted in most prosimian lineages. There are three major arguments for this view. First, the vast majority of extant prosimians are nocturnal. Therefore, the two lemuriform families, Indridae (sifakas) and Lemuridae (true lemurs), are assumed to have become either diurnal or cathemeral only in recent times. Second, the tapetum lucidum, which is a reflecting layer that enhances the ability of the eye to collect light, is found in many strepsirrhines, including some diurnal ones (1). This observation has been taken as evidence that the common ancestor of strepsirrhines had a tapetum and was, therefore, nocturnal. Third, the orbital convergence that is diagnostic of the primate clade is believed to be the result of a nocturnal visualpredator lifestyle (2). Paleontological data, however, are not conclusive about the lifestyle of early primates and suggest the existence of both nocturnal and diurnal forms (3).To explore this issue, we study the opsin genes in prosimians. It is well known that under nocturnality either the short-wavelength (S) or middle-͞long-wavelength (M͞L) opsin will experience relaxed selective constraints and may thus become nonfunctional. Indeed, a nonfunctional S opsin has been found in many nocturnal mammals (4-9). For example, the loss of the S opsin in the raccoon and the kinkajou might have occurred rather quickly because their close diurnal relative, the coati (5, 6), has a functional S opsin. Such a quick loss also is found in Aotus, the only nocturnal simian genus. Aotus diverged from its closest diurnal relatives, the callitrichines (marmosets and tamarins), only Ϸ13-15 million years ago (10). Yet, molecular studies indicate that the loss of the ...

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Section: Resultsmentioning

confidence: 78%

Section: Resultsmentioning

confidence: 90%

See 1 more Smart Citation

Evidence from opsin genes rejects nocturnality in ancestral primates

Tan

Yoder

Yamashita

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

141

132

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“…11-11-02AT). The genomic DNA of a male Bornean tarsier (T. bancanus; n ¼ 1 X chromosome) was extracted from a fibroblast cell line [25].…”

Section: Materials and Methods (A) Study Subjects And Data Collectionmentioning

confidence: 99%

Inferred L/M cone opsin polymorphism of ancestral tarsiers sheds dim light on the origin of anthropoid primates

et al. 2013

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Tarsiers are small nocturnal primates with a long history of fuelling debate on the origin and evolution of anthropoid primates. Recently, the discovery of M and L opsin genes in two sister species, Tarsius bancanus (Bornean tarsier) and Tarsius syrichta (Philippine tarsier), respectively, was interpreted as evidence of an ancestral long-to-middle (L/M) opsin polymorphism, which, in turn, suggested a diurnal or cathemeral (arrhythmic) activity pattern. This view is compatible with the hypothesis that stem tarsiers were diurnal; however, a reversion to nocturnality during the Middle Eocene, as evidenced by hyperenlarged orbits, predates the divergence of T. bancanus and T. syrichta in the Late Miocene. Taken together, these findings suggest that some nocturnal tarsiers possessed high-acuity trichromatic vision, a concept that challenges prevailing views on the adaptive origins of the anthropoid visual system. It is, therefore, important to explore the plausibility and antiquity of trichromatic vision in the genus Tarsius. Here, we show that Sulawesi tarsiers (Tarsius tarsier), a phylogenetic out-group of Philippine and Bornean tarsiers, have an L opsin gene that is more similar to the L opsin gene of T. syrichta than to the M opsin gene of T. bancanus in non-synonymous nucleotide sequence. This result suggests that an L/M opsin polymorphism is the ancestral character state of crown tarsiers and raises the possibility that many hallmarks of the anthropoid visual system evolved under dim (mesopic) light conditions. This interpretation challenges the persistent nocturnal-diurnal dichotomy that has long informed debate on the origin of anthropoid primates.

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“…For instance, nocturnal and solitary strepsirrhines such as the grey mouse lemur (Microcebus murinus; Eberle and Kappeler 2008), the aye-aye (Daubentonia madagascariensis; Sterling and McCreless 2007), and all lorisiformes (Kawamura and Kubotera 2004) rely heavily on olfaction to communicate with other individuals (del Barco-Trillo et al 2011). In general, strepsirrhines also have far less complex visual communication systems than other primates due to poor visibility at night, limited interaction with other individuals and a fused upper lip disallowing facial expression (Kappeler 2012;Kemp and Kaplan 2013).…”

Section: Other Primate Candidates For Learning Human Languagesmentioning

confidence: 99%

Primate social structure as a predictor of modes of communication and the ability to learn a human language

Sullivan¹

2017

The Human Voyage

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For little over five decades, scientists have attempted to teach nonhuman hominids to communicate using human languages . The decision to utilise nonhuman hominids for this area of research is often attributed to their close genetic relatedness and similarly complex social structures to humans (Gardner and Gardner 1978). However, there has been minimal explanation in the literature as to why more complex social group structures allow for successful human language acquisition. Furthermore, there has been no investigation into whether other nonhominid primates, who may be more genetically dissimilar to humans but share similar social group complexity, could also be good candidates for human language acquisition. The following essay will argue that nonhuman hominids are likely successful at human language acquisition as a result of the social complexity hypothesis-a theory that states there is a positive association between social group and communication complexity (Freeberg et al. 2012). It will be proposed that the social complexity hypothesis may also be useful for identifying potential nonhominid candidates for future primate language acquisition research. However, future research should also analyse language acquisition in genera that do not appear to follow the social complexity hypothesis, to determine whether learning human languages requires only social complexity or communication complexity, and not both in combination .

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Ancestral Loss of Short Wave-Sensitive Cone Visual Pigment in Lorisiform Prosimians, Contrasting with Its Strict Conservation in Other Prosimians

Cited by 111 publications

References 38 publications

Evidence from opsin genes rejects nocturnality in ancestral primates

Evidence from opsin genes rejects nocturnality in ancestral primates

Inferred L/M cone opsin polymorphism of ancestral tarsiers sheds dim light on the origin of anthropoid primates

Primate social structure as a predictor of modes of communication and the ability to learn a human language

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