An irregular hourglass pattern describes the tempo of phenotypic development in placental mammal evolution

Abstract

Organismal development is defined by progressive transformations that ultimately give rise to distinct tissues and organs. Thus, temporal shifts in ontogeny often reflect key phenotypic differences in phylogeny. Classical theory predicts that interspecific morphological divergence originates towards the end of embryonic or fetal life stages, i.e. the early conservation model. By contrast, the hourglass model predicts interspecific variation early and late in prenatal ontogeny, though with a phylogenetically similar mid-developmental period. This phylotypic period, however, remains challenging to define within large clades such as mammals. Thus, molecular and morphological tests on a mammalian hourglass have not been entirely congruent. Here, we report an hourglass-like pattern for mammalian developmental evolution. By comparing published data on the timing of 74 homologous characters across 51 placental species, we demonstrated that variation in the timing of development decreased late in embryogenesis––when organ formation is highly active. Evolutionary rates of characters related to this timeframe were lowest, coinciding with a phylotypic period that persisted well beyond the pharyngula ‘stage’. The trajectory culminated with elevated variation in a handful of fetal and perinatal characters, yielding an irregular hourglass pattern. Our study invites further quantification of ontogeny across diverse amniotes and thus challenges current ideas on the universality of developmental patterns.

Shifts in growth, but not differentiation, foreshadow the formation of exaggerated forms under chicken domestication

“…R. Soc. B 288: 20210392 figure S2 and table S2) [30]. We refrained from ranking by the mean of scores owing to the uneven temporal distribution of our sampling (see electronic supplementary material, tables S2-S3).…”

“…Ontogeny can be regarded as a sequence of events which, if altered, can produce novel phenotypic variants [25][26][27]. Evolutionary change in the sequence of some developmental events may occur early in ontogeny and lead to functionally relevant interspecific differences in adults [28][29][30][31]. For example, skeletal traits that arise early on may have longer time to grow and differentiate than those that appear later in ontogeny [32].…”

“…Defining change in ontogenetic sequences (heterochrony) is therefore crucial to informing how phenotypic variation originates [33]. Species-specific differences are generally expected to originate or become apparent near the end of embryonic development [34], presumably because this is when evolutionary change in developmental processes is best incorporated into the ancestrally inherited ontogenetic trajectory [28][29][30]. Within a species, variation is expected to gradually increase towards the end of embryonic development, that is when inductive interactions diminish and tissue components of the organism achieve a greater degree of structural independence or modularity [35,36].…”

Morphological research on amniote eggs and embryos: An introduction and historical retrospective

“…Various studies have used computer‐based methods to analyze and compare the sequence of developmental events in embryos of diverse amniotes and other vertebrate species, and map them onto established phylogenies (Bininda‐Emonds et al, 2002; Jeffery et al, 2005). While questions remain, studies continue to draw on both morphological and molecular data in evaluating the hypotheses (Cordero et al, 2020; Irie, 2017).…”

Domestication and the comparative embryology of birds

“…Beyond chicken, embryology in other domesticated species of Galliformes was also described in the 20th century (Clark, 1960;Fant, 1957;Hendrickx & Hanzlik, 1965;Labisky & Opsahl, 1958;Mun & Kosin, 1960;Smith Padgett & Ivey, 1960;Wilhelm & Robertson, 1941;Williams & Phiillips, 1944). Although domesticated lineages outside of Galliformes were also studied (duck and goose; Cooper & Batt, 1972;Koecke, 1958;Montgomery et al, 1978), the diversity of species in which embryonic development has been studied in detail remains low compared to mammals (Cordero et al, 2020;Hopwood, 2007;Werneburg & Geiger, 2016).…”