Skeletogenesis and sequence heterochrony in rodent evolution, with particular emphasis on the African striped mouse, Rhabdomys pumilio (Mammalia)

Abstract

Data documenting skeletal development in rodents, the most species-rich 'order' of mammals, are at present restricted to a few model species, a shortcoming that hinders exploration of the morphological and ecological diversification of the group. In this study we provide the most comprehensive sampling of rodent ossification sequences to date, with the aim of exploring whether heterochrony is ubiquitous in rodent evolution at the onset of skeletal formation. The onset of ossification in 17 cranial elements and 24 postcranial elements was examined for eight muroid and caviomorph rodent species. New data are provided for two non-model species. For one of these, the African striped mouse, Rhabdomys pumilio, sampling was extended by studying 53 autopodial elements and examining intraspecific variation. The Parsimov method of studying sequence heterochrony was used to explore the role that changes in developmental timing play in early skeletal formation. Few heterochronies were found to diagnose the muroid and caviomorph clades, suggesting conserved patterning in skeletal development. Mechanisms leading to the generation of the wide range of morphological diversity encapsulated within Rodentia may be restricted to later periods in development than those studied in this work. Documentation of skeletogenesis in Rhabdomys indicates that intraspecifc variation in ossification sequence pattern is present, though not extensive. Our study suggests that sequence heterochrony is neither pivotal nor prevalent during early skeletal formation in rodents.

Timing of Ossification in Duck, Quail, and Zebra Finch: lntraspecific Variation, Heterochronies, and Life History Evolution

“…As in the duck, many variations in the sequences affect otic and occipital regions, and the parasphenoid. Plasticity in the development of the autopodia have been reported for other sauropsids such as the Chinese soft-shelled turtle Pelodiscus sinensis (Sánchez-Villagra et al, 2009) or the snapping turtle Chelydra serpentina (Rieppel, 1993; Sheil and Greenbaum, 2005) and at least one more homoeothermic species, the African striped mouse Rhabdomys pumilio (Wilson et al, 2010). …”

“…Bininda-Emonds et al, 2003; Wilson et al, 2010; Weisbecker and Mitgutsch, 2010), could, although they have been discussed as methodological artifacts (Harrison and Larsson, 2008), also hint at high rates of evolutionary changes and thus a sign that many shifts in developmental timing are convergent. Furthermore, given the existence of such high intraspecific variability of ossification, the terminal placements could also be the result of insufficient resolution in taxon sampling.…”

“…Chipman et al, 2000; Maxwell, 2008b; Mitgutsch et al, 2008, 2009; Werneburg and Sánchez-Villagra, in press), suggesting that characteristics in embryonic timing should rather be seen in connection with embryonic anatomy and demands, rather than with those of temporally distant developmental stages (Mitgutsch et al, 2008, 2009). Comparative embryological studies covering different taxa and different character complexes have gathered increasing evidence for intraspecific and, even among closely related taxa, interspecific variability in timing of early embryogenic events (Mabee and Trendler, 1996; Chipman et al, 2000; Moore and Townsend, 2003; Sheil and Greenbaum, 2005; Mitgutsch et al, 2008, 2009; Wilson et al, 2010). When analyzing the timing of such events among distantly related taxa (e.g., Bininda-Emonds et al, 2003; Werneburg and Sánchez-Villagra, 2009; Weisbecker and Mitgutsch, 2010), this intraspecific variability, is reflected in considerable homoplasy and consequently a “terminal branch”-placement of shifts in developmental timing when using algorithms such as event-pair cracking (Jeffery et al, 2002b) and Parsimov (Jeffery et al, 2005).…”

Skeletal development in the African elephant and ossification timing in placental mammals

“…Although they show similarities with other placentals [ [17][18][19][36][37][38], there are some non-artefactual differences in their developmental trajectory: a late ossification of the basioccipital, periotic and phalanges, and an early ossification of the ischium and metacarpals (figure 3).…”

“…Even if Parsimov is commonly viewed as overly conservative [18,19,35], it retrieved similar shifts when either ACCTRAN or DELTRAN analyses were used alone, and to a lesser extent when the strict consensus of the two was used (electronic supplementary material, S3 and S4). Both methods are subject to type II errors owing to the accumulation of ties at early events, which artefactually elevate the 'significance' of early shifts owing to low resolution of the earliest developmental events [17][18][19]36]. Using the Parsimov analysis, it appears that the branch leading to elephant is characterized by a large number of sequence heterochronies, but this abundance of shifts could simply result from the isolation of elephants (as the sole afrotherian) within the presented phylogenetic trees.…”