Adaptive tail-length evolution in deer mice is associated with differential Hoxd13 expression in early development

Variation in the size and number of axial segments underlies much of the diversity in animal body plans. Here, we investigate the evolutionary, genetic, and developmental mechanisms driving tail-length differences between forest and prairie ecotypes of deer mice (Peromyscus maniculatus). We first show that long-tailed forest mice perform better in an arboreal locomotion assay, consistent with tails being important for balance during climbing. The long tails of these forest mice consist of both longer and more caudal vertebrae than prairie mice. Using quantitative genetics, we identify six genomic regions that contribute to differences in total tail length, three of which associate with vertebra length and the other three with vertebra number. For all six loci, the forest allele increases tail length, consistent with the cumulative effect of natural selection. Two of the genomic regions associated with variation in vertebra number contain Hox gene clusters. Of those, we find an allele-specific decrease in Hoxd13 expression in the embryonic tail bud of long-tailed forest mice, consistent with its role in axial elongation. Additionally, we find that forest embryos have more presomitic mesoderm than prairie embryos, and that this correlates with an increase in the number of neuromesodermal progenitors (NMPs), which are modulated by Hox13 paralogs. Together, these results suggest a role for Hoxd13 in the development of natural variation in adaptive morphology on a microevolutionary timescale.

Testing for heterogeneous rates of discrete character evolution on phylogenies

Many hypotheses in the field of phylogenetic comparative biology involve specific changes in the rate or process of trait evolution. We present a method designed to test whether the rate of evolution of a discrete character has changed in one or more clades, lineages, or time periods. This method differs from other related approaches (such as the 'covarion' model) in that the 'regimes' in which the rate or process is postulated to have changed are specified a priori by the user, rather than inferred from the data. Similarly, it differs from methods designed to model a correlation between two binary traits in that the regimes mapped onto the tree are fixed. We apply our method to investigate the rate of dewlap color and/or caudal vertebra number evolution in Caribbean and mainland clades of the diverse lizard genus Anolis. We find little evidence to support any difference between mainland and island evolution in either character. We also examine the statistical properties of the method more generally and show that it has acceptable type I error, parameter estimation, and power. Finally, we discuss the relationship of our method to existing models of heterogeneity in the rate of discrete character evolution on phylogenies.

Differential growth of body segments explains ontogenetic shifts in organ position for the Diamondback Water Snake (Nerodia rhombifer)

As snakes grow, their organs move anteriorly relative to body size. We explored a developmental explanation for the ontogenetic shift in the relative position of internal organs for snakes using the Diamondback Water Snake (Nerodia rhombifer (Hallowell, 1852)). With age, this water snake’s heart, liver, small intestine, and right kidney move anteriorly by 2.5–5.0 percentage points of snout–vent length. The number of precaudal vertebrae did not vary due to size or sex. The anterior edge of the heart, liver, small intestine, and right kidney were typically aligned within a span of 4–8 vertebrae that likewise did not differ as a function of size or sex. Snakes exhibited a positive relationship between the number of precaudal vertebrae and the vertebra number aligned with each organ. Total length, centrum length, centrum width, ball width, height, and mass of eight vertebrae sampled at consistent vertebral number revealed that vertebrae in the middle region of the body grow at a greater rate than vertebrae at the anterior or distal ends of the body. For N. rhombifer, the observed forward shift in relative organ positions is the product of regional differences in the growth of body segments. Predictably, these differences arise from a developmental program generated by the differential expression of Hox genes.