Brain anatomy of two‐toed sloth (Choloepus didactylus, Linnaeus, 1758): A comparative gross anatomical study of extant xenarthrans

Abstract

The neural system plays an important role in understanding some features of animals. Anatomical complexity correlates with the increase of functional capacity. Xenarthrans include anteaters (Vermilingua), armadillos (Cingulata) and sloths (Folivora). This group is the base of eutherian mammals, and understanding the anatomy of its neural system could provide data for functional and evolutionary interpretations. The gross anatomy of the xenarthran brain is recorded. Four extant families of Pilosa and two families of Cingulata were sampled. Usual dissection procedures were used, and the brains were analysed macroscopically. The brain of two‐toed sloth, three‐toed sloth, six‐banded armadillo, giant anteater and collared anteater are gyrencephalic. Pygmy anteater, nine‐banded armadillo, great long‐nosed armadillo, southern naked‐tailed armadillo and giant armadillo are lissencephalic. In most species, the rhinal fissure presents two segments, rostral and caudal (except in Vermilingua and three‐toed sloth). The diencephalon and brainstem present similar anatomy. The cerebellum is wide and presents four lobes (rostral, central, caudal and floccular). Its average volume is 12.16% (Folivora), 14.26% (Vermilingua) and 18.61% (Cingulata). Among these groups, there is a statistical difference between Folivora/Cingulata concerning the cerebellum average. The general pattern of the brain of the xenarthrans is similar to that of other mammals.

Functional or vestigial? The genomics of the pineal gland in Xenarthra

“…For this, we addressed the evolution of a melatoninrelated gene hub, encompassing melatonin synthesis and signaling genes, in Xenarthra and other mammals. Our results strongly suggest a complete landscape of gene loss in Xenarthra, which further reinforce reports suggesting the lack of a pineal gland in several members of this superorder (Quay, 1965;Harlow et al, 1981 , 1994, , Ferrari 1998Freitas 2019). On the other hand, in species in which a pineal gland was described (e.g., Freitas et al, 2019), the present data suggests that, despite the anatomical observations, the canonical pineal gland physiology leading to melatonin secretion is likely disrupted.…”

“…Our results strongly suggest a complete landscape of gene loss in Xenarthra, which further reinforce reports suggesting the lack of a pineal gland in several members of this superorder (Quay, 1965;Harlow et al, 1981 , 1994, , Ferrari 1998Freitas 2019). On the other hand, in species in which a pineal gland was described (e.g., Freitas et al, 2019), the present data suggests that, despite the anatomical observations, the canonical pineal gland physiology leading to melatonin secretion is likely disrupted. Nevertheless, similarly to what was described for Tursiops truncatus (bottlenose dolphin) (Panin et al, 2012), previous radioimmunoassay methods have reported the presence of melatonin circulating in D. novemcinctus (Harlow et al, 1981), implying either the existence of independent pathways for melatonin synthesis and signaling (Slominski et al, 2003;Tan et al, 2016) or possible acquisition of melatonin from food sources (Tan et al, 2010).…”

“…Interestingly, gene loss signatures were identified in these lineages, supporting the loss-of-function of melatonin synthesis, a hallmark of pineal function, and/or signalling (Fang et al, 2014; Huelsmann et al, 2019; Lopes-Marques et al, 2019b), further demonstrating the power of genome analysis towards the clarification of organ function. The presence of a functional pineal gland is also contentious in Xenarthrans (armadillos, anteaters and sloths), a relatively understudied taxonomic group characterized by its intriguing nature (Figure 1; Oksche, 1965; Benítez et al, 1994; Superina & Loughry, 2015; Freitas et al, 2019) and representing one of the earliest-branching clades of placental mammals (Murphy et al, 2007; O’Leary et al, 2013). Xenarthrans are considered imperfect homeotherms, given their poor ability to adjust body temperature (Mc Nab, 1979; 1980; 1985).…”

Functional or Vestigial? The Genomics of the Pineal Gland in Xenarthra

“…Interestingly, gene loss signatures were identified in these lineages, supporting the loss-of-function of melatonin synthesis, a hallmark of pineal function, and/or signalling (Fang et al, 2014;Huelsmann et al, 2019;Lopes-Marques et al, 2019b), further demonstrating the power of genome analysis towards the clarification of organ function. The presence of a functional pineal gland is also contentious in Xenarthrans (armadillos, anteaters and sloths), a relatively understudied taxonomic group characterized by its intriguing nature (Figure 1; Oksche, 1965;Benítez et al, 1994;Superina & Loughry, 2015;Freitas et al, 2019) and representing one of the earliest-branching clades of placental mammals (Murphy et al, 2007;O'Leary et al, 2013). Xenarthrans are considered imperfect homeotherms, given their poor ability to adjust body temperature (Mc Nab, 1979;1980;.…”

“…This inaptitude for thermal regulation, possibly related with their low metabolic rate and low energetic content diet, makes Xenarthrans' activity patterns highly affected by air temperature, with potential effects in their circadian cycles (Chiarello, 1998;Giné et al, 2015;Maccarini et al, 2015;Di Blanco et al, 2017). While a recent report clearly identified pineal glands in the six-banded armadillo (Euphractus sexcintus), Linnaeus's two-toed sloth (Choloepus didactylus), and in the southern tamandua (Tamandua tetradactyla), a distinct pineal was not found or was reported missing in species such as southern long-nosed armadillo (Dasypus hybridus), pale-throated sloth (Bradypus tridactylus), giant anteater (Myrmecophaga tridactyla) or big hairy armadillo (Chaetophractus villosus) (Benítez et al, 1994;Ferrari, 1998;Freitas 2019). However, in the nine-banded armadillo (Dasypus novemcinctus) inconsistent reports advocate for either the presence or absence of a genuine pineal gland (Harlow et al, 1981;Freitas et al, 2019).…”