Getting a head in hard soils: Convergent skull evolution and divergent allometric patterns explain shape variation in a highly diverse genus of pocket gophers (Thomomys).

BACKGROUND: High morphological diversity can occur in closely related animals when selection favors morphologies that are subject to intrinsic biological constraints. A good example is subterranean rodents of the genus Thomomys, one of the most taxonomically and morphologically diverse mammalian genera. Highly procumbent, tooth-digging rodent skull shapes are often geometric consequences of increased body size. Indeed, larger-bodied Thomomys species tend to inhabit harder soils. We used geometric morphometric analyses to investigate the interplay between soil hardness (the main extrinsic selection pressure on fossorial mammals) and allometry (i.e. shape change due to size change; generally considered the main intrinsic factor) on crania and humeri in this fast-evolving mammalian clade. RESULTS: Larger Thomomys species/subspecies tend to have more procumbent cranial shapes with some exceptions, including a small-bodied species inhabiting hard soils. Counter to earlier suggestions, cranial shape within Thomomys does not follow a genus-wide allometric pattern as even regional subpopulations differ in allometric slopes. In contrast, humeral shape varies less with body size and with soil hardness. Soft-soil taxa have larger humeral muscle attachment sites but retain an orthodont (non-procumbent) cranial morphology. In intermediate soils, two pairs of sister taxa diverge through differential modifications on either the humerus or the cranium. In the hardest soils, both humeral and cranial morphology are derived through large muscle attachment sites and a high degree of procumbency. CONCLUSIONS: Our results show that conflict between morphological function and intrinsic allometric patterning can quickly and differentially alter the rodent skeleton, especially the skull. In addition, we found a new case of convergent evolution of incisor procumbency among large-, medium-, and small-sized species inhabiting hard soils. This occurs through different combinations of allometric and non-allometric changes, contributing to shape diversity within the genus. The strong influence of allometry on cranial shape appears to confirm suggestions that developmental change underlies mammalian cranial shape divergences, but this requires confirmation from ontogenetic studies. Our findings illustrate how a variety of intrinsic processes, resulting in species-level convergence, could sustain a genus-level range across a variety of extrinsic environments. This might represent a mechanism for observations of genus-level niche conservation despite species extinctions in mammals.

Phylogenetic structure of the Thomomys bottae-umbrinus complex in North America.

The phylogeography of the Thomomys bottae-umbrinus complex in the United States and Mexico was assessed with sequences of the mitochondrial cytochrome b gene. These sequences were obtained from 225 individuals representing 108 locations over the range, including 56 sequences from GenBank. 110 (500bp) sequences were used for Bayesian inference and neighbor-joining analyses, and 34 (1140bp) specimens from the main clades obtained from the Bayesian inference were used in maximum-parsimony and maximum-likelihood analyses. The different analyses indicate significant variation within the species complex that averages 13% among major groups of genetic differences among Thomomys bottae-umbrinus. The overall pattern of geographic variation is not concordant with the current taxonomy. To the contrary, eight monophyletic groups are supported by all analyses and can be considered phylogenetic species. Overall divergence among these groups appears influenced by historical biogeographic events active during the Pliocene and Pleistocene.

A novel test for host-symbiont codivergence indicates ancient origin of fungal endophytes in grasses.

Significant phylogenetic codivergence between plant or animal hosts (H) and their symbionts or parasites (P) indicates the importance of their interactions on evolutionary time scales. However, valid and realistic methods to test for codivergence are not fully developed. One of the systems where possible codivergence has been of interest involves the large subfamily of temperate grasses (Pooideae) and their endophytic fungi (epichloae). These widespread symbioses often help protect host plants from herbivory and stresses and affect species diversity and food web structures. Here we introduce the MRCALink (most-recent-common-ancestor link) method and use it to investigate the possibility of grass-epichloë codivergence. MRCALink applied to ultrametric H and P trees identifies all corresponding nodes for pairwise comparisons of MRCA ages. The result is compared to the space of random H and P tree pairs estimated by a Monte Carlo method. Compared to tree reconciliation, the method is less dependent on tree topologies (which often can be misleading), and it crucially improves on phylogeny-independent methods such as ParaFit or the Mantel test by eliminating an extreme (but previously unrecognized) distortion of node-pair sampling. Analysis of 26 grass species-epichloë species symbioses did not reject random association of H and P MRCA ages. However, when five obvious host jumps were removed, the analysis significantly rejected random association and supported grass-endophyte codivergence. Interestingly, early cladogenesis events in the Pooideae corresponded to early cladogenesis events in epichloae, suggesting concomitant origins of this grass subfamily and its remarkable group of symbionts. We also applied our method to the well-known gopher-louse data set.