Making a bat: The developmental basis of bat evolution

Bats are incredibly diverse, both morphologically and taxonomically. Bats are the only mammalian group to have achieved powered flight, an adaptation that is hypothesized to have allowed them to colonize various and diverse ecological niches. However, the lack of fossils capturing the transition from terrestrial mammal to volant chiropteran has obscured much of our understanding of bat evolution. Over the last 20 years, the emergence of evo-devo in non-model species has started to fill this gap by uncovering some developmental mechanisms at the origin of bat diversification. In this review, we highlight key aspects of studies that have used bats as a model for morphological adaptations, diversification during adaptive radiations, and morphological novelty. To do so, we review current and ongoing studies on bat evolution. We first investigate morphological specialization by reviewing current knowledge about wing and face evolution. Then, we explore the mechanisms behind adaptive diversification in various ecological contexts using vision and dentition. Finally, we highlight the emerging work into morphological novelties using bat wing membranes.

Keywords:
Chiroptera; wing; craniofacial; sensory adaptations; teeth

Authorship

Alexa Sadier ^*Send correspondence to Alexa Sadier. University of California at Los Angeles, Department of Ecology and Evolutionary Biology, Los Angeles, USA. E-mail: asadier@ucla.edu.

University of California at Los Angeles, Department of Ecology and Evolutionary Biology, Los Angeles, USA. University of California at Los AngelesUSALos Angeles, USAUniversity of California at Los Angeles, Department of Ecology and Evolutionary Biology, Los Angeles, USA.

Daniel J. Urban ^*Send correspondence to Daniel J. Urban. University of California at Los Angeles, Department of Ecology and Evolutionary Biology, Los Angeles, USA. E-mail: djurban2@ucla.edu.

American Museum of Natural History, Department of Mammalogy, New York, USA.American Museum of Natural HistoryUSANew York, USAAmerican Museum of Natural History, Department of Mammalogy, New York, USA.

Neal Anthwal

Aidan O. Howenstine

Ishani Sinha

Karen E. Sears

http://orcid.org/0000-0001-9744-9602

Send correspondence to
Alexa Sadier. University of California at Los Angeles, Department of Ecology and Evolutionary Biology, Los Angeles, USA. E-mail: asadier@ucla.edu.

Send correspondence to
Daniel J. Urban. University of California at Los Angeles, Department of Ecology and Evolutionary Biology, Los Angeles, USA. E-mail: djurban2@ucla.edu.

Associate Editor:

Igor Schneider

Conflict of Interest

The authors declare that there is no conflict of interest that could be perceived as prejudicial to the impartiality of the reported research.

Author Contributions

AS, DJU, NA, AOH and KES conveived the idea and wrote the manuscript; IS wrote the manuscript. All authors read and approved the final version.

SCIMAGO INSTITUTIONS RANKINGS

Figures

Figures (5)

Thumbnail

Figure 1 -
Phylogeny of bats. (a) Cladogram* showing intraordinal phylogenetic relationships in Chiroptera (adapted from Teeling et al., 2018Teeling EC, Vernes SC, Dávalos LM, Ray DA, Gilbert MTP, Myers E and Bat1K Consortium (2018) Bat biology, genomes, and the Bat1K Project: To generate chromosome-level genomes for all living bat species. Annu Rev Anim Biosci 6:23-46.). Based on molecular data, Chiroptera is now classified into Yinpterochiroptera (orange) and Yangochiroptera (magenta), while the traditional classification into microbats and megabats is shown in grey. (b) Cladogram* showing the interordinal relationship between Chiroptera and other mammalian taxa (adapted from Jebb et al., 2020Jebb D, Huang Z, Pippel M, Hughes GM, Lavrichenko K, Devanna P, Winkler S, Jermiin LS, Skirmuntt EC, Katzourakis A, et al. (2020) Six new reference-quality bat genomes illuminate the molecular basis and evolution of bat adaptations. Nature 583:578-584.). Three of the best supported tree topologies for the relationship between the Laurasiatherian lineages Carnivora, Perrissodactyla, Cetartiodactyla, Pholidota and Chiroptera (indicated by shaded area) are shown. *Branch lengths do not indicate distance.

Thumbnail

Figure 2 -
Differences in signaling centers between bat and mouse limb development. Larger expression domains in bat AER and ZPA, combined with a feedback loop caused by later re-initiation of Fgf8 and Shh, contributes to lengthening in bat forelimbs (reproduced from Cooper and Sears, 2013Cooper LN and Sears KE (2013) How to grow a bat wing. In: Adams R and Pederson S (eds) Bat evolution, ecology, and conservation Springer, New York, pp 3-20.).

Thumbnail

Figure 3 -
Color vision diversity in Phyllostomids (adapted from Sadier et al., 2018Rossoni DM, Assis APA, Giannini NP and Marroig G (2017) Intense natural selection preceded the invasion of new adaptive zones during the radiation of New World leaf-nosed bats. Sci Rep 7:11076.). Cones are shown on flat-mounted retinas in four different bat species representative of the cone diversity in Phyllostomids. To visualize L opsin (green) and S opsin (magenta), flat-mounted retinas were probed with two antibodies against L and S opsins. L opsin expressing cones were found in all bats, while S opsins were only seen in fruit visiting Carollia and Artibeus species, indicating cone type and diversity vary between species occupying different dietary niches. Diet is indicated with a pictogram.

Thumbnail

Figure 4 -
Jaw and dental diversity of Noctilionoid bats. Members of the group occupy every possible dietary niche found in bats. In line with this, jaw size and shape as well as tooth shape, size and proportion are highly variable in Noctilionoid bats. In fact, the jaw and tooth types shown represent most of the breadth of the diversity found in both bat superfamilies. Diet is indicated with a pictogram. Scale: 10 mm

Thumbnail

Figure 5 -
The anatomy and development of the bat wing (a) Outline of extended forelimb and wing membranes in chiropterans demonstrating the skeleton and membranes (patagia) of the wing (from Swartz et al., 1996Steeman ME, Hebsgaard MB, Fordyce RE, Ho SYW, Rabosky DL, Nielsen R, Rahbek C, Glenner H, Sorensen MV and Willerslev E (2009) Radiation of extant cetaceans driven by restructuring of the oceans. Syst Biol 58:573-585.). (b) Examples of variation in size and shape of patagia (from Norberg and Rayner, 1987Norberg UM and Rayner JMV (1987) Ecological morphology and flight in bats (Mammalia; Chiroptera): Wing adaptations, flight performance, foraging Strategy and echolocation. PhilosTrans R Soc Lond B Biol Sci 316:335-427. ). (c) Early limb development in bats compared to mice showing early similarities in limb development and divergence in growth and maturation. (from Cretekos et al., 2008 Cretekos CJ , Wang Y, Green ED, Martin JF, Rasweiler JJ and Behringer RR (2008) Regulatory divergence modifies limb length between mammals. Genes Dev 22:141-151.).

Figure 1 - Phylogeny of bats. (a) Cladogram* showing intraordinal phylogenetic relationships in Chiroptera (adapted from **Teeling et al., 2018**Teeling EC, Vernes SC, Dávalos LM, Ray DA, Gilbert MTP, Myers E and Bat1K Consortium (2018) Bat biology, genomes, and the Bat1K Project: To generate chromosome-level genomes for all living bat species. Annu Rev Anim Biosci 6:23-46.). Based on molecular data, Chiroptera is now classified into Yinpterochiroptera (orange) and Yangochiroptera (magenta), while the traditional classification into microbats and megabats is shown in grey. (b) Cladogram* showing the interordinal relationship between Chiroptera and other mammalian taxa (adapted from **Jebb et al., 2020**Jebb D, Huang Z, Pippel M, Hughes GM, Lavrichenko K, Devanna P, Winkler S, Jermiin LS, Skirmuntt EC, Katzourakis A, et al. (2020) Six new reference-quality bat genomes illuminate the molecular basis and evolution of bat adaptations. Nature 583:578-584.). Three of the best supported tree topologies for the relationship between the Laurasiatherian lineages Carnivora, Perrissodactyla, Cetartiodactyla, Pholidota and Chiroptera (indicated by shaded area) are shown. *Branch lengths do not indicate distance.

Figure 2 - Differences in signaling centers between bat and mouse limb development. Larger expression domains in bat AER and ZPA, combined with a feedback loop caused by later re-initiation of Fgf8 and Shh, contributes to lengthening in bat forelimbs (reproduced from Cooper and Sears, 2013Cooper LN and Sears KE (2013) How to grow a bat wing. In: Adams R and Pederson S (eds) Bat evolution, ecology, and conservation Springer, New York, pp 3-20.).

Figure 3 - Color vision diversity in Phyllostomids (adapted from **Sadier et al., 2018**Rossoni DM, Assis APA, Giannini NP and Marroig G (2017) Intense natural selection preceded the invasion of new adaptive zones during the radiation of New World leaf-nosed bats. Sci Rep 7:11076.). Cones are shown on flat-mounted retinas in four different bat species representative of the cone diversity in Phyllostomids. To visualize L opsin (green) and S opsin (magenta), flat-mounted retinas were probed with two antibodies against L and S opsins. L opsin expressing cones were found in all bats, while S opsins were only seen in fruit visiting Carollia and Artibeus species, indicating cone type and diversity vary between species occupying different dietary niches. Diet is indicated with a pictogram.

Figure 4 - Jaw and dental diversity of Noctilionoid bats. Members of the group occupy every possible dietary niche found in bats. In line with this, jaw size and shape as well as tooth shape, size and proportion are highly variable in Noctilionoid bats. In fact, the jaw and tooth types shown represent most of the breadth of the diversity found in both bat superfamilies. Diet is indicated with a pictogram. Scale: 10 mm

Figure 5 - The anatomy and development of the bat wing (a) Outline of extended forelimb and wing membranes in chiropterans demonstrating the skeleton and membranes (patagia) of the wing (from **Swartz et al., 1996Steeman ME, Hebsgaard MB, Fordyce RE, Ho SYW, Rabosky DL, Nielsen R, Rahbek C, Glenner H, Sorensen MV and Willerslev E (2009) Radiation of extant cetaceans driven by restructuring of the oceans. Syst Biol 58:573-585.). (b) Examples of variation in size and shape of patagia (from Norberg and Rayner, 1987Norberg UM and Rayner JMV (1987) Ecological morphology and flight in bats (Mammalia; Chiroptera): Wing adaptations, flight performance, foraging Strategy and echolocation. PhilosTrans R Soc Lond B Biol Sci 316:335-427. ). (c) Early limb development in bats compared to mice showing early similarities in limb development and divergence in growth and maturation. (from Cretekos et al., 2008** Cretekos CJ , Wang Y, Green ED, Martin JF, Rasweiler JJ and Behringer RR (2008) Regulatory divergence modifies limb length between mammals. Genes Dev 22:141-151.).

How to cite

copy

Sociedade Brasileira de Genética Rua Cap. Adelmio Norberto da Silva, 736, 14025-670 Ribeirão Preto SP Brazil, Tel.: (55 16) 3911-4130 / Fax.: (55 16) 3621-3552 - Ribeirão Preto - SP - Brazil
E-mail: editor@gmb.org.br

Acompanhe os números deste periódico no seu leitor de RSS

Versão para download de PDF

PDF

Inglês

Versões e tradução automática

Versão original do texto

English

Tradução automática

Google Translator
Microsoft Translator

Como citar

RIS

BIBTEX

Outros formatos de citação e exportação:

SciELO - Scientific Electronic Library Online
Rua Dr. Diogo de Faria, 1087 – 9º andar – Vila Clementino 04037-003 São Paulo/SP - Brasil
E-mail: scielo@scielo.org

Leia a Declaração de Acesso Aberto

Métricas

Making a bat: The developmental basis of bat evolution

PlumX

Mensagem

[1] Send correspondence to
Alexa Sadier. University of California at Los Angeles, Department of Ecology and Evolutionary Biology, Los Angeles, USA. E-mail: asadier@ucla.edu.