Creating diversity in mammalian facial morphology: a review of potential developmental mechanisms

Abstract

Mammals (class Mammalia) have evolved diverse craniofacial morphology to adapt to a wide range of ecological niches. However, the genetic and developmental mechanisms underlying the diversification of mammalian craniofacial morphology remain largely unknown. In this paper, we focus on the facial length and orofacial clefts of mammals and deduce potential mechanisms that produced diversity in mammalian facial morphology. Small-scale changes in facial morphology from the common ancestor, such as slight changes in facial length and the evolution of the midline cleft in some lineages of bats, could be attributed to heterochrony in facial bone ossification. In contrast, large-scale changes of facial morphology from the common ancestor, such as a truncated, widened face as well as the evolution of the bilateral cleft possessed by some bat species, could be brought about by changes in growth and patterning of the facial primordium (the facial processes) at the early stages of embryogenesis.

Differential cellular proliferation underlies heterochronic generation of cranial diversity in phyllostomid bats

“…At the cellular level, elevated proliferation rate in committed progenitors may trigger terminal cell divisions to occur earlier, likely at CS18, which can then lead to a shorter or truncated face. This is in contrast to short-face morphology resulting from deficient outgrowth of the facial processes, the proximate mechanism proposed by Usui and Tokita [71]. We note that since A. jamaicensis is a basal branching member of the short-face fruit-eating bats, the more extreme shortfaced fruit bats may indeed undergo additional heterochronic shifts as described by Usui and Tokita, 2018, but currently no data from morphometric studies support this potential paedomorphic change.…”

Normal embryonic development of the greater horseshoe bat Rhinolophus ferrumequinum, with special reference to nose leaf formation

“…The class Mammalia (mammals), which is composed of 29 major clades, contains over 5,400 extant species (Feldhamer, Drickamer, Vessey, Merritt, & Krajewski, ; Kemp, ; Vaughan, Ryan, & Czaplewski, ; Wilson & Reeder, ). Mammals have evolved diverse body shapes through adaptation to a variety of environments (Usui & Tokita, ). Embryological study is one of the most effective approaches to understanding how this morphological diversity arose in mammalian evolutionary history since the process of animal shape formation can be directly observed.…”

“…Embryological study is one of the most effective approaches to understanding how this morphological diversity arose in mammalian evolutionary history since the process of animal shape formation can be directly observed. To date, the molecular and cellular mechanisms that regulate mammalian body plan formation have been described through a series of studies on laboratory mice (see Table of Usui & Tokita, ). However, the developmental mechanisms that create morphological diversity in mammals have been only partially understood.…”

“…Bat craniofacial morphology is highly diverse, corresponding to their adaptation to various environments. Ernst Haeckel, an influential comparative embryologist and an artist in the nineteenth century, published impressive artwork of chiropteran craniofacial diversity (Haeckel, ; Usui & Tokita, ). The New World leaf‐nosed bats (family Phyllostomidae) are a good example showing incredible diversity of facial morphology (Baker, Bininda‐Emonds, Mantilla‐Meluk, Porter, & Van Den Bussche, ; Dumont, , ; Dumont et al, ; Santana, Grosse, & Dumont, ; Sears, ; Usui & Tokita, ).…”

“…The horseshoe bats (family Rhinolophidae) and Old World leaf‐nosed bats (family Hipposideridae), closely related members of the clade Yinpterochiroptera, are known for their well‐developed and complex nose‐leaves (Usui & Tokita, ; Vaughan et al, ). Although the nose‐leaves possessed by other bat families are generally a simple leaf‐like structure composed of a thin epithelial membrane, those of rhinolophids, and hipposiderids are elaborate epithelial structures composed of three parts: a smooth baffle (horseshoe plate) that occupies approximately the ventral three‐fourths of the epithelial appendage, a dorsally projected central spike adjacent to the upper rim of the nostrils, and a posterior leaf dorsal to the central spike (Figure ).…”