Heterochrony revisited: the evolution of developmental sequences

The concept of heterochrony is a persistent component of discussions about the way that evolution and development interact. Since the late 1970s heterochrony has been defined largely as developmental changes in the relationship of size and shape. This approach to heterochrony, here termed growth heterochrony, is limited in the way it can analyse change in the relative timing of developmental events in a number of respects. In particular, analytical techniques do not readily allow the study of changes in developmental events not characterized by size and shape parameters, or of many kinds of events in many taxa. I discuss here an alternative approach to heterochrony, termed sequence heterochrony, in which a developmental trajectory is conceptualized as a series of discrete events. Heterochrony is demonstrated when the sequence position of an event changes relative to other events in that sequence. I summarize several analytical techniques that allow the investigation of sequence heterochrony in phylogenetic contexts and also quantitatively. Finally, several examples of how this approach may be used to test hypotheses on the way development evolves are summarized.     

Complete Mitochondrial Genomes and Eutherian Evolution

Recent large-scale nuclear DNA phylogenies have supported unconventional interordinal relationships among modern eutherians as well as divergence dates (100 mya) that substantially predate the first appearance of fossils from modern eutherians near the Cretaceous/Cenozoic (K/T) boundary (65-70 mya). For comparison to the nuclear data, I analyzed 12 complete mitochondrial DNA (mtDNA) protein-coding genes (10,677 bp) from 53 eutherian taxa, using maximum-likelihood methods to estimate model parameters (GTR + I + ) and to optimize topology and branch-length estimates. Although closely resembling the nuclear DNA trees, the mtDNA maximum-likelihood tree is just one of seven statistically indistinguishable ( lnL 1.747) trees, each suggesting different evolutionary relationships. This 53-taxon data set and another including 56 taxa provide no statistically significant support for a monophyletic afrotherian clade. In fact, these mitochondrial DNA sequences fail to support the monophyly of three putative eutherian divisions suggested by the nuclear data (Afrotheria, Laurasiatheria or Euarchontoglires). By comparison to well-supported branches describing relationships among families, those describing interordinal relationships are extremely short and only tenuously supported. Neither these sequences, nor sequences simulated under a known tree, fully resolve any interordinal relationship. Even simulated sequences that are twice as long (22kb) as mtDNA protein-coding genes are too short and too saturated to resolve the deepest and shortest interordinal relationships. Further, the mammalian mtDNA sequences appear to depart significantly from molecular-clock and quartet dating assumptions. Unlike recent nuclear DNA studies, I find that mtDNA genes, by themselves, are inadequate to describe relationships or divergence times at the base of the eutherian tree.     

New basal eutherian mammal from the Early Cretaceous Jehol biota,Liaoning, China

A new genus and species of eutherian mammal, Acristatherium yanensis gen. et sp. nov., is described from the Early Cretaceous Jehol biota, China. The new taxon is based on a partial skull that is preserved in three dimensions from the Lujiatun bed of the Yixian Formation and dated 123.2±1.0 Ma. Its right upper and lower dentitions are nearly complete and it has a dental formula 4.1.5.3/3.1.5.3. The new mammal reveals several craniodental characteristics of Early Cretaceous eutherians previously unknown in fossil records of therians, such as a possible vestige of the septomaxilla. The craniodental features of the new taxon are compared with those of relevant Early Cretaceous eutherians and therians. Phylogenetic analyses based on a data matrix containing 70 taxa and 408 characters place A. yanensis as the most basal eutherian in the selected group. The morphological differences between Acristatherium and Eomaia indicate that eutherians already had a significant degree of generic diversification ca 125 Ma.     

湖北万朝山自然保护区兽类调查报告及保护

2005年8月对湖北万朝山兽类物种多样性、兽类特点、兽类生存环境等做了调查,为万朝山拟建立国家级自然保护区提出兽类物种多样性保护性建议。万朝山有兽类62种,隶属于7目、23科,其中国家Ⅰ级保护兽类3种,国家Ⅱ级保护兽类11种;与湖北省其它保护区相比,万朝山兽类生存环境小气候特征显著。     

Scaling of the marsupial middle ear and its functional significance

The marsupial middle ear performs an anatomical impedance matching for acoustic energy travelling in air to reach the cochlea. The size of the middle ear sets constraints for the frequencies transmitted. For generalized placental mammals, it has been shown that the limit for high-frequency hearing can be predicted on the basis of middle ear ossicle mass, provided that the ears fulfil requirements of isometry. We studied the interspecific size variation of the middle ear in 23 marsupial species, with the following measurable parameters: skull mass, condylobasal length, ossicular masses for malleus, incus and stapes, tympanic membrane area, oval window area, and lever arm lengths for malleus and incus. Our results show that the middle ear size grows with negative allometry in relation to body size and that the internal proportions of the marsupial middle ear are largely isometric. This resembles the situation in placental mammals and allows us to use their isometric middle ear model to predict the high-frequency hearing limit for marsupials. We found that the isometry model predicts the high-frequency hearing limit for different marsupials well, indicating that marsupials can be used as auditory models for general therian mammalian hearing. At very high frequencies, other factors, such as the inner ear, seem to constrain mammalian hearing.     

Can reintroductions to degraded habitat succeed? A test using the common brushtail possum

Habitat degradation contributes to species decline, and habitat quality is an important factor influencing reintroduction success globally. Habitat quality can include a range of physical resources such as nest sites and food resources but also anything that can restrict the use of these resources such as predation risk or competition. In arid Australia, introduced predators are thought to be the primary cause of mammal extinction and reintroduction failure although habitat clearance and alteration are also major causes of population decline. Common brushtail possums are one arid Australian marsupial close to regional extinction. To understand whether habitat quality was limiting their recovery, we reintroduced 148 possums into an area where introduced red foxes were controlled but historic overgrazing had degraded the habitat. We measured both direct (hollow availability, midstorey cover and high‐quality plant foods) and indirect (survival, condition, reproduction, movement) measures of habitat quality. Sixty‐seven released possums and 26 post‐release recruits were radiocollared for up to 2 years after release. Post‐release survival of radiocollared possums was high after 12 months (0.70), and there were no deaths from starvation. Predation by feral cats was the most common cause of mortality, and the open, degraded habitat may have exacerbated predation risk. Continuous breeding, good body condition and comparative home ranges with other sites suggested that food resources were not limiting. Possums used natural tree hollows in Eucalyptus spp. with no use of artificial nest boxes. Results suggest that historically degraded habitat was not a barrier to short‐term reintroduction success when foxes were controlled and natural tree hollows were plentiful. However, demographic data on hollow‐bearing tree species suggest a possible future decline in availability of hollows. These factors, combined with the unknown effects of drought, and synergistic effects of predation and poor quality habitat, suggest long‐term reintroduction success may require improved habitat and cat control.     

Comparative phylogenetic analysis of blcap/nnat reveals eutherian-specific imprinted gene

Imprinted genes are parent-of-origin dependent, monoallelically expressed genes present in marsupials and eutherian mammals. Altered expression of imprinted genes plays a significant role in the etiology of a variety of human disorders and diseases. Nevertheless, the regulatory mechanisms of imprinting remain poorly defined. The imprinted gene Neuronatin (Nnat) is an excellent candidate for studying imprinting because it resides within the 8.5-kb intron of the nonimprinted gene Bladder Cancer-Associated Protein (Blcap) and is the only imprinted gene within the region. A phylogenetic comparison of this micro-imprinted domain in human, mouse, and rat revealed several candidates for imprint control, including tandem repeats and putative binding sites for trans- acting factors known to be involved in chromatin remodeling. Genome-wide phylogenetic comparisons of species from the three major extant mammalian clades failed, however, to show any evidence of Nnat outside the eutherian lineage. Thus, Nnat is the first identified eutherian-specific imprinted gene, demonstrating that imprinted genes did not arise at a single point during evolution. This finding also suggests that the complexity of imprinting regulation observed at other loci may, in part, be directly related to the amount of time they have been imprinted.     

Rates of genome evolution and branching order from whole genome analysis

Accurate estimation of any phylogeny is important as a framework for evolutionary analysis of form and function at all levels of organization from sequence to whole organism. Using alignments of nonrepetitive components of opossum, human, mouse, rat, and dog genomes we evaluated two alternative tree topologies for eutherian evolution. We show with very high confidence that there is a basal split between rodents (as represented by the mouse and rat) and a branch joining primates (as represented by humans) and carnivores (as represented by dogs), consistent with some but not the most widely accepted mammalian phylogenies. The result was robust to substitution model choice with equivalent inference returned from a spectrum of models ranging from a general time reversible model, a model that treated nucleotides as either purines and pyrimidines, and variants of these that incorporated rate heterogeneity among sites. By determining this particular branching order we are able to show that the rate of molecular evolution is almost identical in rodent and carnivore lineages and that sequences evolve approximately 11%-14% faster in these lineages than in the primate lineage. In addition by applying the chicken as outgroup the analyses suggested that the rate of evolution in all eutherian lineages is approximately 30% slower than in the opossum lineage. This pattern of relative rates is inconsistent with the hypothesis that generation time is an important determinant of substitution rates and, by implication, mutation rates. Possible factors causing rate differences between the lineages include differences in DNA repair and replication enzymology, and shifts in nucleotide pools. Our analysis demonstrates the importance of using multiple sequences from across the genome to estimate phylogeny and relative evolutionary rate in order to reduce the influence of distorting local effects evident even in relatively long sequences.