Prenatal postcranial development in two species of sympatric Japanese wood mice (<i>Apodemus argenteus</i> and <i>A. speciosus</i>): a comparison of arboreal versus terrestrial congeners
Abstract:Habitats of two closely related Japanese field mice, Apodemus argenteus and A. speciosus, broadly overlap in many Japanese forests. A. argenteus being more arboreal and
A. speciosus being more terrestrial, it is thought that such ecological segregation allows their sympatric distribution. Comparing these two congeners, whether ecological difference is reflected in postcranial
development was examined. Although overall ossification sequences were virtually identical, development of the caudal vertebrae was rema… Show more
“…This led them to conclude that the common ancestor of extant bats was possibly a sophisticated echolocator and that laryngeal echolocation emerged just once. Given the evidence that prenatal development of skeletons is evolutionary labile and heterochronies are highly common among mammals (Kuhn & Zeller, ; Koyabu et al, ; Koyabu & Son, ; Koyabu, ; Werneburg et al, ; Zeller, ), whether the quantitative traits of a common ancestor can simply be inferred from fetuses of extant species is questionable. Meanwhile, regardless of the applicability of Haeckel's law of recapitulation, at the very least, Wang et al's () interpretation that fetal growth is similar between non‐laryngeal echolocators and laryngeal echolocators cannot be drawn from their dataset since only a limited number of fetal stages were collected and only a few aspects of cochlear growth were compared in their study.…”
Cochlear morphology has been regarded as one of the key traits to understand the origin and evolution of echolocation in bats, given its functionality and performance for receiving echolocation sonar. While numerous researchers have compared adult-stage morphology, few have studied the prenatal development of the cochlea. Here, we provide the first detailed three-dimensional description of the prenatal cranial development in bats, using Rhinolophus thomasi as a model, with particular interest to the petrosal which houses the cochlea. Results revealed that among all cranial bones the onset of the ossification of the petrosal is earlier in R. thomasi when compared to other reported mammals. Generally, the cochlea reaches adult size and shape before or around birth in placental mammals including bats, but we found that its shape and size growths continue until maturity in Rhinolophus species. The relationship of cochlear size and skull size is maintained constant throughout the postnatal ontogeny to adulthood in Rhinolophus, a pattern previously reported neither in any other bats nor other mammals. The peculiar developmental pattern in Rhinolophus possibly allows them to form their characteristically large cochlea and facilitate their distinctive echolocation behavior. A recent study reported that non-echolocating Pteropodidae shares a similar prenatal cochlear size to laryngeal echolocating bats. The apparent resemblance of fetal cochlear size was proposed to be a vestigial signal of large cochlear size in the last common ancestor of bats and thus as supporting evidence for the single origin of laryngeal echolocation. However, results from the present observations suggest that limited aspects of the cochlear development were captured in this previous investigation and that the resulting interpretations may be questionable. We point out that diversity and patterns of cochlear development among bats are still not resolved, and the controversy on the origins of laryngeal echolocation is still open to discussion.
“…This led them to conclude that the common ancestor of extant bats was possibly a sophisticated echolocator and that laryngeal echolocation emerged just once. Given the evidence that prenatal development of skeletons is evolutionary labile and heterochronies are highly common among mammals (Kuhn & Zeller, ; Koyabu et al, ; Koyabu & Son, ; Koyabu, ; Werneburg et al, ; Zeller, ), whether the quantitative traits of a common ancestor can simply be inferred from fetuses of extant species is questionable. Meanwhile, regardless of the applicability of Haeckel's law of recapitulation, at the very least, Wang et al's () interpretation that fetal growth is similar between non‐laryngeal echolocators and laryngeal echolocators cannot be drawn from their dataset since only a limited number of fetal stages were collected and only a few aspects of cochlear growth were compared in their study.…”
Cochlear morphology has been regarded as one of the key traits to understand the origin and evolution of echolocation in bats, given its functionality and performance for receiving echolocation sonar. While numerous researchers have compared adult-stage morphology, few have studied the prenatal development of the cochlea. Here, we provide the first detailed three-dimensional description of the prenatal cranial development in bats, using Rhinolophus thomasi as a model, with particular interest to the petrosal which houses the cochlea. Results revealed that among all cranial bones the onset of the ossification of the petrosal is earlier in R. thomasi when compared to other reported mammals. Generally, the cochlea reaches adult size and shape before or around birth in placental mammals including bats, but we found that its shape and size growths continue until maturity in Rhinolophus species. The relationship of cochlear size and skull size is maintained constant throughout the postnatal ontogeny to adulthood in Rhinolophus, a pattern previously reported neither in any other bats nor other mammals. The peculiar developmental pattern in Rhinolophus possibly allows them to form their characteristically large cochlea and facilitate their distinctive echolocation behavior. A recent study reported that non-echolocating Pteropodidae shares a similar prenatal cochlear size to laryngeal echolocating bats. The apparent resemblance of fetal cochlear size was proposed to be a vestigial signal of large cochlear size in the last common ancestor of bats and thus as supporting evidence for the single origin of laryngeal echolocation. However, results from the present observations suggest that limited aspects of the cochlear development were captured in this previous investigation and that the resulting interpretations may be questionable. We point out that diversity and patterns of cochlear development among bats are still not resolved, and the controversy on the origins of laryngeal echolocation is still open to discussion.
“…It is worth noting that Haeckel himself was aware and acknowledged that embryos can only provide a portrait of ancestral conditions and that this may apply to limited cases (Richardson & Keuck, 2002). Given the numerous evidence that prenatal development is evolutionary labile and heterochrony is highly common among vertebrates (Hautier et al, 2013; Hugi et al, 2012; Koyabu & Son, 2014; Koyabu et al, 2011; Koyabu, 2017; Kuhn & Zeller, 1987; Spiekman & Werneburg, 2017; Werneburg & Sánchez‐Villagra, 2015; Zeller, 1987), the idea that the quantitative traits of a common ancestor can simply be inferred from fetuses of extant species is highly questionable. Although there are a few cases that fit with Haeckel's recapitulation theory (e.g., Lovejoy, 2000; Nagashima et al, 2009), they only apply to certain traits of certain stages, and it must be remembered that there are at the same time various examples that refute Haeckel's proposition (Alberch, 1985; de Beer, 1937).…”
Section: Discussionmentioning
confidence: 99%
“…In their report, Haeckel's recapitulation theory was adopted as the base of their evolutionary extrapolation, but there is little evidence that ancestral conditions can be simply inferred from the prenatal development of extant species (Richardson & Keuck, 2002). Instead, it is widely accepted that prenatal development is evolutionarily highly variable even between closely related species (Koyabu, 2017; Koyabu & Son, 2014; Koyabu et al, 2011, 2014; Werneburg & Sánchez‐Villagra, 2015). Although in some certain cases prenatal development may show ancestral conditions that are lost in extant taxa (Koyabu et al, 2012; Richardson & Keuck, 2002), this does not guarantee that all events or processes of prenatal development should be treated as characters of ancestral taxa (de Beer, 1958).…”
Haeckel's recapitulation theory has been a controversial topic in evolutionary biology. However, we have seen some recent cases applying Haeckel's view to interpret the interspecific variation of prenatal ontogeny. To revisit the validity of Haeckel's recapitulation theory, we take bats that have undergone drastic morphological changes and possess a characteristic ecology as a case study. All members of Rhinolophoidea and Yangochiroptera can generate an ultrasonic pulse from the larynx to interpret surrounding objects (laryngeal echolocation) whereas Pteropodidae lacks such ability. It is known that the petrosal bone is particularly derived in shape and expanded in laryngeal echolocators. If Haeckel's recapitulation theory holds, the formation of this derived trait should occur later than those of other bones. Therefore, we compared the prenatal ossification timing of the petrosal in 15 bat species and five outgroup species. We found that the ossification of the petrosal is accelerated in laryngeal echolocators while it is the last bone to ossify in non‐laryngeal echolocating bats and non‐volant mammals, which runs counter to the prediction generated by Haeckel's recapitulation theory. We point out the evolutionarily labile nature of trait developmental timing and emphasize that Haeckel's recapitulation theory does not hold in many cases. We caution that generating predictions on ancestral conditions and evolutionary history leading from Haeckel's recapitulation theory is not well supported.
“…However, the functional significance of ossification heterochrony is largely unstudied, despite the considerable interspecific diversity of the ossification sequence reported to date [96]. Some studies have linked ossification heterochrony to evolutionary changes in relative bone sizes [96–98], but many refuting examples exist, and empirical data is still largely lacking [99–102]. Figure 9Example of ossification sequence in greater short-nosed fruit bat ( Cynopterus sphinx ).…”
Section: Evolution Of the Mammalian Skull Developmentmentioning
In the last decade, studies integrating palaeontology, embryology and experimental developmental biology have markedly altered our homological understanding of the mammalian skull. Indeed, new evidence suggests that we should revisit and restructure the conventional anatomical terminology applied to the components of the mammalian skull. Notably, these are classical problems that have remained unresolved since the ninteenth century. In this review, I offer perspectives on the overlooked problems associated with the homology, development, and conservatism of the mammalian skull, aiming to encourage future studies in these areas. I emphasise that ossification patterns, bone fusion, cranial sutures and taxon-specific neomorphic bones in the skull are virtually unexplored, and further studies would improve our homological understanding of the mammalian skull. Lastly, I highlight that overlooked bones may exist in the skull that are not yet known to science and suggest that further search is needed.
This article is part of the theme issue ‘The mammalian skull: development, structure and function’.
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