Canalization and developmental stability of the yellow-necked mouse (Apodemus flavicollis) mandible and cranium related to age and nematode parasitism

Vida Jojić,Borislav Čabrilo,Vladimir M Jovanović,Jelena Blagojević,Olivera Bjelić-Čabrilo,Mladen Vujošević,Ivana Budinski

doi:10.1186/s12983-021-00439-4

Vida Jojić, Borislav Čabrilo + Show 5 more

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https://doi.org/10.1186/s12983-021-00439-4

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Abstract

BackgroundMammalian mandible and cranium are well-established model systems for studying canalization and developmental stability (DS) as two elements of developmental homeostasis. Nematode infections are usually acquired in early life and increase in intensity with age, while canalization and DS of rodent skulls could vary through late postnatal ontogeny. We aimed to estimate magnitudes and describe patterns of mandibular and cranial canalization and DS related to age and parasite intensity (diversity) in adult yellow-necked mice (Apodemus flavicollis).ResultsWe found the absence of age-related changes in the levels of canalization for mandibular and cranial size and DS for mandibular size. However, individual measures of mandibular and cranial shape variance increased, while individual measures of mandibular shape fluctuating asymmetry (FA) decreased with age. We detected mandibular and cranial shape changes during postnatal ontogeny, but revealed no age-related dynamics of their covariance structure among and within individuals. Categories regarding parasitism differed in the level of canalization for cranial size and the level of DS for cranial shape. We observed differences in age-related dynamics of the level of canalization between non-parasitized and parasitized animals, as well as between yellow-necked mice parasitized by different number of nematode species. Likewise, individual measures of mandibular and cranial shape FA decreased with age for the mandible in the less parasitized category and increased for the cranium in the most parasitized category.ConclusionsOur age-related results partly agree with previous findings. However, no rodent study so far has explored age-related changes in the magnitude of FA for mandibular size or mandibular and cranial FA covariance structure. This is the first study dealing with the nematode parasitism-related canalization and DS in rodents. We showed that nematode parasitism does not affect mandibular and cranial shape variation and covariance structure among and within individuals. However, parasite intensity (diversity) is related to ontogenetic dynamics of the levels of canalization and DS. Overall, additional studies on animals from natural populations are required before drawing some general conclusions.

Highlights

Mammalian mandible and cranium are well-established model systems for studying canalization and developmental stability (DS) as two elements of developmental homeostasis
First age category (A1)—first age category, Second age category (A2)—second age category, Third age category (A3)—third age category according to Jovanović et al yyyy[66]; Non-parasitized animals (P0)—non-parasitized animals, Animals parasitized by one nematode species (P1)—animals parasitized by one nematode species, Animals parasitized by two nema‐ tode species (P2)—animals parasitized by two nematode species, P3— animals parasitized by three to five nematode species. m—males, f—females; B0—animals with standard karyotype, B chromosomes (Bs) + – animals with Bs of host mice, estimated from dry eye lens weight
Age categories—Size Parametric F-tests in analysis of variance (ANOVA) of centroid size (CS) reveal that mandibular and cranial size variation among individuals, as well as directional asymmetry (DA) and fluctuating asymmetry (FA) for the mandible, are all highly significant in all age categories (Additional file 2: Table S2)

Summary

Introduction

Mammalian mandible and cranium are well-established model systems for studying canalization and developmental stability (DS) as two elements of developmental homeostasis. And functionally complex morphological structures, such as mammalian mandible and cranium, are well-established model systems for studying canalization, developmental stability (DS), and morphological integration, recognized by Hallgrímsson et al [1] as three main components of phenotypic variability. The key distinction between them is in the origin of potential factors contributing to phenotypic variation in such a way that environmental perturbations arise outside of an individual, while developmental noise, as stochastic fluctuations in developmental processes, arises within an individual [1, 7,8,9]. Developmental noise is not caused by environmental or genetic variation, environmental and genetic factors can affect developmental processes that mediate its expression and influence DS [9, 10]

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