Skip to main content
Advertisement

Main menu

  • Home
  • Articles
    • Accepted manuscripts
    • Issue in progress
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Interviews
    • Sign up for alerts
  • About us
    • About JEB
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Outstanding paper prize
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contact JEB
    • Subscriptions
    • Advertising
    • Feedback
    • Institutional usage stats (logged-in users only)
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

User menu

  • Log in

Search

  • Advanced search
Journal of Experimental Biology
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

supporting biologistsinspiring biology

Journal of Experimental Biology

  • Log in
Advanced search

RSS  Twitter  Facebook  YouTube  

  • Home
  • Articles
    • Accepted manuscripts
    • Issue in progress
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Interviews
    • Sign up for alerts
  • About us
    • About JEB
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Outstanding paper prize
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contact JEB
    • Subscriptions
    • Advertising
    • Feedback
    • Institutional usage stats (logged-in users only)
SHORT COMMUNICATION
Sex reversal induces size and performance differences among females of the African pygmy mouse, Mus minutoides
Samuel Ginot, Julien Claude, Julie Perez, Frederic Veyrunes
Journal of Experimental Biology 2017 220: 1947-1951; doi: 10.1242/jeb.157552
Samuel Ginot
Institut des Sciences de l'Evolution de Montpellier, Universite de Montpellier, CNRS, IRD, Cc 064; Place Eugene Bataillon, Montpellier Cedex 5 34095, France
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for Samuel Ginot
  • For correspondence: samuel.ginot@umontpellier.fr
Julien Claude
Institut des Sciences de l'Evolution de Montpellier, Universite de Montpellier, CNRS, IRD, Cc 064; Place Eugene Bataillon, Montpellier Cedex 5 34095, France
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Julie Perez
Institut des Sciences de l'Evolution de Montpellier, Universite de Montpellier, CNRS, IRD, Cc 064; Place Eugene Bataillon, Montpellier Cedex 5 34095, France
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Frederic Veyrunes
Institut des Sciences de l'Evolution de Montpellier, Universite de Montpellier, CNRS, IRD, Cc 064; Place Eugene Bataillon, Montpellier Cedex 5 34095, France
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • Article
  • Figures & tables
  • Info & metrics
  • PDF
Loading

This article has a correction. Please see:

  • Correction: Sex reversal induces size and performance differences among females of the African pygmy mouse, Mus minutoides (doi: 10.1242/jeb.157552) - May 15, 2018

ABSTRACT

Differences in biological performance, at both intra- and inter-specific levels, have often been linked to morphology but seldom to behavioural or genotypic effects. We tested performance at the intraspecific level by measuring bite force in the African pygmy mouse, Mus minutoides. This species displays an unusual sex determination system, with sex-reversed, X*Y females carrying a feminizing X* chromosome. X*Y females cannot be differentiated from XX females based on external or gonadal morphology; however, they are known to be more aggressive. We found that bite force was higher in X*Y females than in other females and males. We then performed geometric morphometric analyses on their skulls and mandibles and found that the higher performance of X*Y females was mainly explained by a greater overall skull size. The effects of the X* chromosome thus go beyond feminization, and extend to whole-organism performance and morphology. Our results also suggest limited effects of behaviour on bite force.

INTRODUCTION

Bite force is a frequently used performance trait in functional morphological studies. Most of these studies have clearly demonstrated the link between osteology, muscular activity and biting performance at the intraspecific as well as interspecific levels (e.g. Herrel et al., 1999; Aguirre et al., 2002; Davis et al., 2010; Santana et al., 2010). Morphology has also been shown to be a driver of performance and fitness via intra-sexual competition (Herrel et al., 2010; Lailvaux et al., 2004). However, to our knowledge, the interactions between genetics, behaviour, morphology and performance at the intraspecific and even intra-sex levels have not yet been studied in mammals.

Here, we investigated bite force and skull morphology in the African pygmy mouse, Mus (Nannomys) minutoides Smith 1834. This species is known to have a unusual sex determination system, with three types of sex chromosomes: X, Y and a feminizing X*, producing XY males and XX, XX* females and a high proportion of sex-reversed, X*Y females (Veyrunes et al., 2010). The three types of females present no differences in external morphology or gonad anatomy (Rahmoun et al., 2014), but are known to vary in other traits: X*Y females have a higher reproductive success (Saunders et al., 2014), and have a much more aggressive behaviour (latency to attack, number of attacks; Saunders et al., 2016) than the XX and XX* females. Because biting is one of the characteristics of attacks that relates to aggressiveness, we compared the bite force of the X*Y females with that of other females and males to assess the effect of their genotypic changes on performance. In parallel, we performed measurements of morphological attributes of the skull and mandible in all genotypes. By doing so, we tried to link chromosomal differences to performance, through potential morphological and/or behavioural (aggressiveness) variations. Examining these interactions in M. minutoides could also help improve our understanding of the ecological and evolutionary implications of the emergence of this unusual sex determination system.

MATERIALS AND METHODS

Specimens

All mice were raised in the facilities of Montpellier University (France). The colony was established from wild-caught animals from South Africa (see details in Saunders et al., 2014). Overall, 54 mice were used in the experiments with 19 males and 35 females, all adults. Seventeen females were found to carry a Y chromosome using PCR amplification of the Sry gene (following Veyrunes et al., 2010). The 18 others did not have the Sry gene, and thus were either XX or XX*. XX and XX* females do not differ in terms of behaviour and reproductive success (Saunders et al., 2014, 2016) and were pooled in this study after checking that they did not represent distinct phenotypic groups. Recognizing all XX* females requires karyotyping, which is technically demanding; instead, we were able to identify eight of them in our dataset thanks to their genealogy. These eight individuals were compared with the other non-X*Y females, and their morphology and bite force were roughly equivalent in mean and variance (results not shown). These XX and XX* females are hereby referred to as ‘XX females’. The experimental protocol was performed in accordance with European guidelines and with the approval of the Ethical Committee on Animal Care and Use of France (no. CEEA-LR-12170).

Bite force measurements

Bite force was measured using a piezoelectric force transducer (Herrel et al., 1999; Aguirre et al., 2002). Measurements were performed prior to PCR amplification, avoiding user-behaviour bias, and by a single user, to avoid inter-user error. Each mouse bit three times in a row and the highest bite force was selected for analysis. Group means were compared using Tukey's HSD test. The mice were then euthanized by CO2 inhalation, and kept at −20°C until further treatment.

Morphometric geometrics and statistical analyses

All skulls were cleaned manually and kept in the collections of Montpellier University. Eleven landmarks were digitized on the dorsal side of the skull, and 16 on the mandible using the software tpsDig2.0 (Fig. 1A,B). Landmark data were imported and analyzed in R (R Foundation for Statistical Computing, Vienna, Austria), using the procrustes superimposition method, with functions from Claude (2008). Missing landmarks (owing to the fragility of the mandible), if any, were estimated using a tps interpolation. Centroid sizes of the skulls and mandibles were computed and used as the size variables (Bookstein, 1991). Principal component analyses (PCAs) were run on superimposed coordinates to check for shape differences between males, XX females and X*Y females. In all analyses, the PC axes retained represented 90% of shape variation. A type II ANOVA was run to test the effects of sex chromosomal group, age, size and their interactions on bite force. For shape, several models were fitted with a different sum of squares partitioning (Table 1), and MANOVAs were used to assess the influence of sex chromosomal groups on the principal components of shape variation.

Fig. 1.
  • Download figure
  • Open in new tab
  • Download powerpoint
Fig. 1.

Geometric morphometric analyses of the skull and mandible of the males, XX females and X*Y females of Mus minutoides. Landmarks for (A) the skull and (B) the mandible of Mus minutoides. (C) PCA based on the landmark data for the skull, with PC1 representing 16.4% and PC2, 15.3% of the variation. (D) PCA for the mandible, with 10.8% and 9% of the variation displayed by PC1 and PC2, respectively. Black triangles are males (n=19), green crosses are X*Y females (n=17) and red plus signs are XX females (n=18). Skull and mandible shapes on the right of the graph represent minimal (black) and maximal (red) shapes along the PC axes. No significant shape differences were found between these groups. For the skull, positive values on PC1 represent a narrower skull with a longer snout but a shorter braincase, while negative values represent a broader skull with a shorter snout and a longer braincase. On PC2, positive values have a shorter snout and a wider inter-orbital region in comparison to negative values. For the mandible, positive values on PC1 correspond to overall flatter mandibles, with the angular process more posteriorly developed, while the coronoid process is shorter and in a more anterior position than for negative values. On PC2, positive values correspond to mandibles with a shorter molar row, more posterior coronoid process, shorter condylar process and longer angular process than negative values.

View this table:
  • View inline
  • View popup
  • Download powerpoint
Table 1.

Results of the ANOVA and MANOVAs run on bite force and morphology of Mus minutoides

RESULTS AND DISCUSSION

X*Y females bit significantly harder than other females (Fig. 2; data are available on request from the corresponding author). They also bit harder than males, but not significantly so; bite force was similar between males and XX females. Table 2 shows the results of the Tukey's HSD test.

Fig. 2.
  • Download figure
  • Open in new tab
  • Download powerpoint
Fig. 2.

Boxplot of bite forces of the three M. minutoides groups. Data are shown for males (n=19), XX females (n=18) and X*Y females (n=17). Limits of the boxes represent the upper and lower quartiles, the bar is the median, the whiskers represent the maximum and minimum value, or 1.5 times the interquartile distance in cases where outliers are present, and the circles are outliers. Asterisks indicate significant differences between means. Tukey's HSD test revealed a significant increase in bite force in X*Y females compared with XX females (P<0.01).

View this table:
  • View inline
  • View popup
  • Download powerpoint
Table 2.

Results of Tukey's HSD test for differences in bite force, mandible centroid size and skull centroid size

No major morphological differences appeared between the three groups,which overlapped in morphospace (Fig. 1C,D, Table 1).

X*Y females displayed a significantly greater centroid size than males and XX females (Table 2), even independently of age (Table 1). MANOVAs did not reveal any effect of the group on shape; however, they showed significant allometry shared by all groups (Table 1).

There was a significant size–bite force correlation (r≈0.6, d.f.=52, P<0.01 for both bones) when considering the data as a whole (i.e. not taking the groups into account). A relationship was also found between age and bite force (r=0.3, d.f.=49, P<0.05). In the linear model created, the type II ANOVA revealed that, once age and size were taken into account, bite force differences were no longer significant between the groups (F=1.28, d.f.=2, den. d.f.=42, P>0.2), although the tendency for X*Y females to have higher bite force than XX remained. In this model, age had no significant effect, and size remained the main explanatory variable.

We showed that in the African pygmy mouse, X*Y females bite harder than the XX females and, more surprisingly, also bite harder than males (although not significantly so). Limited shape variation between the sex chromosomal groups (Fig. 1C,D) shows that skull and mandible shape are not at the root of the higher bite force of X*Y females. It also suggests that the presence of the Y and/or X* chromosomes does not significantly influence shape. However, without considering the groups, we found a positive relationship between size and bite force, as shown in previous studies (Herrel et al., 2001; Lailvaux et al., 2004; Freeman and Lemen, 2008). Furthermore, X*Y females displayed a greater skull size, which appears to explain part of their increased bite force (Tables 1, 2). Performance changes independent of size but owing to behavioural differences between the groups are subtle and not significant, suggesting that aggressiveness has a much lower impact on performance variation than morphological determininants (here size).

Hormones are also known to influence performance, as demonstrated by hormonal and molecular screening of elite female athletes, which detected sex development disorders with hyperandrogenism (e.g. XY females) in an occurrence 200 times greater than in the general population (e.g. Fénichel et al., 2013). In our model, however, the M. minutoides X*Y females harbour typical ovarian anatomy (no ovotestes) and a normal anogenital distance, suggesting a low level of circulating androgen (Rahmoun et al., 2014), observations that have been recently confirmed by preliminary hormonal assays on testosterone (F.V., unpublished data). Therefore, the increased skull size of X*Y females appears to be the main cause of their higher bite force.

Although not much is known about the ecology of M. minutoides (Britton-Davidian et al., 2012), the advantages of having higher performance may be twofold. Higher bite force may increase the range of available food resources (Aguirre et al., 2003) by allowing the X*Y individuals to feed on harder food. Second, higher aggressiveness coupled with stronger bites may have a role in intra-sex competition: X*Y females may increase their reproductive success by taking dominance over other females via attacks (Lailvaux and Irschick, 2006). This has been shown for lizards, in which dominance, territorial defense and the outcome of fights are all linked to performance (Herrel et al., 2010; Lailvaux et al., 2004).

Chromosomal changes in the X*Y females may thus give them a dominant position, consistent with the hypothesis that an increase in fitness explains the maintenance of these females, despite the costly loss of the unviable YY embryos (Saunders et al., 2014). Considering our results and those of Saunders et al. (2014, 2016), it appears that the X*Y females obtain selective advantages through many aspects of their fitness: reproductive success, behaviour and whole-organism performance. The effect of the X* chromosome thus goes well beyond feminization, and is at the origin of a complex and multi-factorial X* syndrome that extends to life history traits, behaviour (Saunders et al., 2014, 2016), size variation and performance (present study). Interestingly, these X*Y females were characterized as ‘super females’ because they were shown to have a better reproductive output than the XX females (Saunders et al., 2014), but in addition, they present hyper-masculinized traits with an enhanced aggressiveness, larger skulls and stronger bite forces than males. It is notoriously hard to assign performance modifications to naturally occurring genetic changes, but this model offers a fantastic framework with which to further connect performance, morphology, behaviour and sex chromosomes.

Acknowledgements

The authors thank the CECEMA animal facility. We also thank Paul A. Saunders for his comments on the manuscript. We are grateful to A. Herrel and one anonymous reviewer for their insightful comments. This publication is a contribution of the Institut des Sciences de l'Evolution de Montpellier (UMR 5554 – UM2+CNRS+IRD+EPHE) No. ISEM 2017-055.

FOOTNOTES

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: S.G., J.C., F.V.; Methodology: S.G., J.C., J.P., F.V.; Formal analysis: S.G., J.C.; Investigation: S.G., J.P., F.V.; Resources: S.G., J.C., F.V.; Writing - original draft: S.G.; Writing - review & editing: S.G., J.C., F.V.; Supervision: J.C., F.V.

  • Funding

    This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.

  • Received February 1, 2017.
  • Accepted March 16, 2017.
  • © 2017. Published by The Company of Biologists Ltd
http://www.biologists.com/user-licence-1-1/

References

  1. ↵
    1. Aguirre, L. F.,
    2. Herrel, A.,
    3. van Damme, R. and
    4. Matthysen, E.
    (2002). Ecomorphological analysis of trophic niche partitioning in a tropical savannah bat community. Proc. R. Soc. Lond. B Biol. Sci. 269, 1271-1278. doi:10.1098/rspb.2002.2011
    OpenUrlAbstract/FREE Full Text
  2. ↵
    1. Aguirre, L. F.,
    2. Herrel, A.,
    3. Van Damme, R. and
    4. Matthysen, E.
    (2003). The implications of food hardness for diet in bats. Funct. Ecol. 17, 201-212. doi:10.1046/j.1365-2435.2003.00721.x
    OpenUrlCrossRef
  3. ↵
    1. Bookstein, F. L.
    (1991). Morphometric Tools for Landmark Data. Cambridge: Cambridge University Press.
  4. ↵
    1. Britton-Davidian, J.,
    2. Robinson, T. J. and
    3. Veyrunes, F.
    (2012). Systematics and evolution of the African pygmy mice, subgenus Nannomys: a review. Acta Oecolog. 42, 41-49. doi:10.1016/j.actao.2012.01.001
    OpenUrlCrossRef
  5. ↵
    1. Claude, J.
    (2008). Morphometrics with R. New York: Springer Science & Business Media.
  6. ↵
    1. Davis, J. L.,
    2. Santana, S. E.,
    3. Dumont, E. R. and
    4. Grosse, I. R.
    (2010). Predicting bite force in mammals: two-dimensional versus three-dimensional lever models. J. Exp. Biol. 213, 1844-1851. doi:10.1242/jeb.041129
    OpenUrlAbstract/FREE Full Text
  7. ↵
    1. Fénichel, P.,
    2. Paris, F.,
    3. Philibert, P.,
    4. Hiéronimus, S.,
    5. Gaspari, L.,
    6. Kurzenne, J. Y.,
    7. Chevallier, P.,
    8. Bermon, S.,
    9. Chevalier, N. and
    10. Sultan, C.
    (2013). Molecular diagnosis of 5alpha-reductase deficiency in 4 elite young female athletes through hormonal screening for hyperandrogenism. J. Clin. Endocrinol. Metabol. 98, E1055-E1059. doi:10.1210/jc.2012-3893
    OpenUrlCrossRefPubMedWeb of Science
  8. ↵
    1. Freeman, P. W. and
    2. Lemen, C. A.
    (2008). A simple morphological predictor of bite force in rodents. J. Zool. 275, 418-422. doi:10.1111/j.1469-7998.2008.00459.x
    OpenUrlCrossRef
  9. ↵
    1. Herrel, A.,
    2. Spithoven, L.,
    3. Van Damme, R. and
    4. De Vree, F.
    (1999). Sexual dimorphism of head size in Gallotia galloti: testing the niche divergence hypothesis by functional analyses. Funct. Ecol. 13, 289-297. doi:10.1046/j.1365-2435.1999.00305.x
    OpenUrlCrossRefWeb of Science
  10. ↵
    1. Herrel, A.,
    2. Van Damme, R.,
    3. Vanhooydonck, B. and
    4. De Vree, F.
    (2001). The implications of bite performance for diet in two species of lacertid lizards. Can. J. Zool. 79, 662-670. doi:10.1139/z01-031
    OpenUrlCrossRefWeb of Science
  11. ↵
    1. Herrel, A.,
    2. Moore, J. A.,
    3. Bredeweg, E. M. and
    4. Nelson, N. J.
    (2010). Sexual dimorphism, body size, bite force and male mating success in tuatara. Biol. J. Linn Soc. 100, 287-292. doi:10.1111/j.1095-8312.2010.01433.x
    OpenUrlCrossRef
  12. ↵
    1. Lailvaux, S. P. and
    2. Irschick, D. J.
    (2006). A functional perspective on sexual selection: insights and future prospects. Anim. Behav. 72, 263-273. doi:10.1016/j.anbehav.2006.02.003
    OpenUrlCrossRefWeb of Science
  13. ↵
    1. Lailvaux, S. P.,
    2. Herrel, A.,
    3. VanHooydonck, B.,
    4. Meyers, J. J. and
    5. Irschick, D. J.
    (2004). Performance capacity, fighting tactics and the evolution of life–stage male morphs in the green anole lizard (Anolis carolinensis). Proc. R. Soc. B Biol. Sci. 271, 2501-2508. doi:10.1098/rspb.2004.2891
    OpenUrlAbstract/FREE Full Text
  14. ↵
    1. Rahmoun, M.,
    2. Perez, J.,
    3. Saunders, P. A.,
    4. Boizet-Bonhoure, B.,
    5. Wilhelm, D.,
    6. Poulat, F. and
    7. Veyrunes, F.
    (2014). Anatomical and molecular analyses of XY ovaries from the African pygmy mouse Mus minutoides. Sex. Dev. 8, 356-363. doi:10.1159/000368664
    OpenUrlCrossRef
  15. ↵
    1. Santana, S. E.,
    2. Dumont, E. R. and
    3. Davis, J. L.
    (2010). Mechanics of bite force production and its relationship to diet in bats. Funct. Ecol. 24, 776-784. doi:10.1111/j.1365-2435.2010.01703.x
    OpenUrlCrossRefWeb of Science
  16. ↵
    1. Saunders, P. A.,
    2. Perez, J.,
    3. Rahmoun, M.,
    4. Ronce, O.,
    5. Crochet, P.-A. and
    6. Veyrunes, F.
    (2014). XY females do better than the XX in the African pygmy mouse, Mus minutoides. Evolution 68, 2119-2127. doi:10.1111/evo.12387
    OpenUrlCrossRef
  17. ↵
    1. Saunders, P. A.,
    2. Franco, T.,
    3. Sottas, C.,
    4. Maurice, T.,
    5. Ganem, G. and
    6. Veyrunes, F.
    (2016). Masculinised behaviour of XY females in a mammal with naturally occuring sex reversal. Sci. Rep. 6, 22881. doi:10.1038/srep22881
    OpenUrlCrossRef
  18. ↵
    1. Veyrunes, F.,
    2. Chevret, P.,
    3. Catalan, J.,
    4. Castiglia, R.,
    5. Watson, J.,
    6. Dobigny, G.,
    7. Robinson, T. J. and
    8. Britton-Davidian, J.
    (2010). A novel sex determination system in a close relative of the house mouse. Proc. R. Soc. B Biol. Sci. 277, 1049-1056. doi:10.1098/rspb.2009.1925
    OpenUrlAbstract/FREE Full Text
Previous ArticleNext Article
Back to top
Previous ArticleNext Article

This Issue

Keywords

  • Behaviour
  • Bite force
  • Geometric morphometrics
  • Intra-sex competition
  • Sex reversal

 Download PDF

Email

Thank you for your interest in spreading the word on Journal of Experimental Biology.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Sex reversal induces size and performance differences among females of the African pygmy mouse, Mus minutoides
(Your Name) has sent you a message from Journal of Experimental Biology
(Your Name) thought you would like to see the Journal of Experimental Biology web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
SHORT COMMUNICATION
Sex reversal induces size and performance differences among females of the African pygmy mouse, Mus minutoides
Samuel Ginot, Julien Claude, Julie Perez, Frederic Veyrunes
Journal of Experimental Biology 2017 220: 1947-1951; doi: 10.1242/jeb.157552
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
SHORT COMMUNICATION
Sex reversal induces size and performance differences among females of the African pygmy mouse, Mus minutoides
Samuel Ginot, Julien Claude, Julie Perez, Frederic Veyrunes
Journal of Experimental Biology 2017 220: 1947-1951; doi: 10.1242/jeb.157552

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Alerts

Please log in to add an alert for this article.

Sign in to email alerts with your email address

Article navigation

  • Top
  • Article
    • ABSTRACT
    • INTRODUCTION
    • MATERIALS AND METHODS
    • RESULTS AND DISCUSSION
    • Acknowledgements
    • FOOTNOTES
    • References
  • Figures & tables
  • Info & metrics
  • PDF

Related articles

Cited by...

More in this TOC section

  • High carbohydrate diet ingestion increases post-meal lipid synthesis and drives respiratory exchange ratios above 1
  • Tokay geckos (Gekkonidae: Gekko gecko) preferentially use substrates that elicit maximal adhesive performance
  • Rapid toxin sequestration modifies poison frog physiology
Show more SHORT COMMUNICATION

Similar articles

Other journals from The Company of Biologists

Development

Journal of Cell Science

Disease Models & Mechanisms

Biology Open

Advertisement

Welcome to JEB’s new Editor Monica Daley

We are pleased to welcome Monica Daley to JEB’s Editorial team. Monica has had a long association with JEB before taking up her new role, overseeing peer review of neuromuscular physiology, terrestrial biomechanics and integrative physiology of locomotion.


In the field with Robyn Hetem

Continuing our fieldwork series, Robyn Hetem reflects on working with species ranging from aardvark to zebra, and the impact COVID-19 has had on fieldwork.


Read & Publish participation continues to grow

“It is particularly encouraging for early career researchers, as it allows them to display their research globally without the need to find costs to cover the open access option.”

Professor Fernando Montealegre-Z (University of Lincoln) shares his experience of publishing Open Access as part of our growing Read & Publish initiative. We now have over 150 institutions in 15 countries and four library consortia taking part – find out more and view our full list of participating institutions.


Nocturnal reef residents have deep-sea-like eyes

Fanny de Busserolles and colleagues from The University of Queensland have discovered that the eyes of nocturnal reef fish have multibank retinas, layers of photoreceptors, similar to the eyes of deep-sea fish that live in dim light conditions.


Mechanisms underlying gut microbiota–host interactions in insects

In their Review, Konstantin Schmidt and Philipp Engel summarise recent findings about the mechanisms involved in gut colonisation and the provisioning of beneficial effects in gut microbiota–insect symbiosis.

Articles

  • Accepted manuscripts
  • Issue in progress
  • Latest complete issue
  • Issue archive
  • Archive by article type
  • Special issues
  • Subject collections
  • Interviews
  • Sign up for alerts

About us

  • About JEB
  • Editors and Board
  • Editor biographies
  • Travelling Fellowships
  • Grants and funding
  • Journal Meetings
  • Workshops
  • The Company of Biologists
  • Journal news

For Authors

  • Submit a manuscript
  • Aims and scope
  • Presubmission enquiries
  • Article types
  • Manuscript preparation
  • Cover suggestions
  • Editorial process
  • Promoting your paper
  • Open Access
  • Outstanding paper prize
  • Biology Open transfer

Journal Info

  • Journal policies
  • Rights and permissions
  • Media policies
  • Reviewer guide
  • Sign up for alerts

Contact

  • Contact JEB
  • Subscriptions
  • Advertising
  • Feedback

 Twitter   YouTube   LinkedIn

© 2021   The Company of Biologists Ltd   Registered Charity 277992