Parent–offspring similarity in the timing of developmental events: an origin of heterochrony?

Abstract

Understanding the link between ontogeny (development) and phylogeny (evolution) remains a key aim of biology. Heterochrony, the altered timing of developmental events between ancestors and descendants, could be such a link although the processes responsible for producing heterochrony, widely viewed as an interspecific phenomenon, are still unclear. However, intraspecific variation in developmental event timing, if heritable, could provide the raw material from which heterochronies originate. To date, however, heritable developmental event timing has not been demonstrated, although recent work did suggest a genetic basis for intraspecific differences in event timing in the embryonic development of the pond snail, Radix balthica. Consequently, here we used high-resolution (temporal and spatial) imaging of the entire embryonic development of R. balthica to perform a parent -offspring comparison of the timing of twelve, physiological and morphological developmental events. Between-parent differences in the timing of all events were good predictors of such timing differences between their offspring, and heritability was demonstrated for two of these events (foot attachment and crawling). Such heritable intraspecific variation in developmental event timing could be the raw material for speciation events, providing a fundamental link between ontogeny and phylogeny, via heterochrony.

Heterokairy: a significant form of developmental plasticity?

“…While this approach may be difficult for groups such as mammals whose embryos undergo protected development, there are good models to be found among other groups such as invertebrates and some fish whose embryonic development occurs in external, transparent eggs. Recent technological developments have also allowed the high-resolution video imaging of such embryos, which makes the measurement of physiological events tractable [67].…”

“…For example, it might be predicted that the earlier expression of a 'costly' trait could affect traits occurring later in development [66] with implications for life-history strategies. Here, the use of inbred lines for developmental events that have been shown to be heritable [67] would be an effective resource, as would species for which heterochronic genes have been identified [68]. Finally, the approach of factoring sequence heterochrony into the study of developmental plasticity could also be extended to include tests of quantitative genetic models for evolutionary change during development, including the potential role of epigenetic effects [69].…”

Variance in developmental event timing is greatest at low biological levels: implications for heterochrony

“…Most studies of heterochrony have concentrated on documenting differences in developmental event timing between species, with an implicit assumption that any within-species variation is minor, and probably not relevant to addressing questions relating to this macroevolutionary pattern. However, evidence for intraspecific differences in developmental event timing is accumulating (Cubbage & Mabee, 1996;Mabee & Trendler, 1996;Mabee, Olmstead & Cubbage, 2000;Schmidt & Starck, 2004;Sheil & Greenbaum, 2005;de Jong et al, 2009;Kawajiri, Kokita & Yamahira, 2009), in addition to the findings of a study by Tills et al (2011Tills et al ( , 2013 highlighting that such inter-individual variation could have a genetic basis. Given that intraspecific variation in developmental event timing may be biologically important, it is timely to begin addressing how this variation is partitioned at different biological levels to begin to appreciate the implications of such intraspecific variation for our understanding of heterochrony.…”

“…For example, we know little about variation at different biological levels during development; indeed, variation during development has often been viewed as 'noise' that hampers the investigation of the genetic control of developmental processes (Spicer & Gaston, 1999;. However, an emerging body of evidence is revealing significant intraspecific variation during development, including variation in the timing of developmental events at the individual level (Gomez-Mestre et al, 2008de Jong et al, 2009;Mourabit et al, 2010;Pan & Burggren, 2010;Tills et al, 2011;Tills, Rundle & Spicer, 2013).…”

Differences in the timing of cardio-respiratory development determine whether marine gastropod embryos survive or die in hypoxia

“…When such intraspecific altered timing occurs as a result of the influence of environmental factors, it is a form of developmental plasticity termed heterokairy (Spicer and Burggren, 2003;Spicer and Rundle, 2007). Heterokairy has been proposed as a potential mechanistic basis for the evolutionary pattern of heterochrony -differences in developmental timing between ancestors and their descendants (Tills et al, 2013;Mueller et al, 2015). At the same time, it may be of ecological importance, allowing species to tolerate and/or survive stressful environmental conditions.…”