Integration, heterochrony, and adaptation in pedal digits of syndactylous marsupials

Background. Marsupial syndactyly is a curious morphology of the foot found in all species of diprotodontian and peramelemorph marsupials. It is traditionally defined as a condition in which digits II and III of the foot are bound by skin and are reduced. Past treatments of marsupial syndactyly have not considered the implications of this unique morphology for broader issues of digit development and evolution, and the ongoing debate regarding its phylogenetic meaning lacks a broad empirical basis. This study undertakes the first interdisciplinary characterisation of syndactyly, using variance/covariance matrix comparisons of morphometric measurements, locomotor indices, ossification sequences, and re-assessment of the largely anecdotal data on the phylogenetic distribution of tarsal/metatarsal articulations and "incipient syndactyly". Results. Syndactylous digits have virtually identical variance/covariance matrices and display heterochronic ossification timing with respect to digits IV/V. However, this does not impact on overall locomotor adaptation patterns in the syndactylous foot as determined by analysis of locomotor predictor ratios. Reports of incipient syndactyly in some marsupial clades could not be confirmed; contrary to previous claims, syndactyly does not appear to impact on tarsal bone arrangement. Conclusion. The results suggest that marsupial syndactyly originates from a constraint that is rooted in early digit ontogeny and results in evolution of the syndactylous digits as a highly integrated unit. Although convergent evolution appears likely, syndactyly in Diprotodontia and Peramelemorpha may occur through homologous developmental processes. We argue that the term "syndactyly" is a misnomer because the marsupial condition only superficially resembles its name-giving human soft-tissue syndactyly

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. KEYWORDS: Environmental selection pressure; Evolutionary development; Heterochrony; Incisor procumbency; Parallel evolution; Principal component analysis; Repeated evolution; Subterranean nich

Governance:Governance Frameworks for Wastewater Management

MVZ specimen catalog numbers and views represented. (XLSX 495 kb

Relative demographic susceptibility does not explain the extinction chronology of Sahul's megafauna

The causes of Sahul's megafauna extinctions remain uncertain, although several interacting factors were likely responsible. To examine the relative support for hypotheses regarding plausible ecological mechanisms underlying these extinctions, we constructed the first stochastic, age-structured models for 13 extinct megafauna species from five functional/taxonomic groups, as well as 8 extant species within these groups for comparison. Perturbing specific demographic rates individually, we tested which species were more demographically susceptible to extinction, and then compared these relative sensitivities to the fossil-derived extinction chronology. Our models show that the macropodiformes were the least demographically susceptible to extinction, followed by carnivores, monotremes, vombatiform herbivores, and large birds. Five of the eight extant species were as or more susceptible than the extinct species. There was no clear relationship between extinction susceptibility and the extinction chronology for any perturbation scenario, while body mass and generation length explained much of the variation in relative risk. Our results reveal that the actual mechanisms leading to the observed extinction chronology were unlikely related to variation in demographic susceptibility per se, but were possibly driven instead by finer-scale variation in climate change and/or human prey choice and relative hunting success.Peer reviewe

Out on a limb: bandicoot limb co-variation suggests complex impacts of development and adaptation on marsupial forelimb evolution

SUMMARY Marsupials display far less forelimb diversity than placentals, possibly because of the laborious forelimb-powered climb to the pouch performed by most marsupial neonates. This is thought to result in stronger morphological integration (i.e., higher co-variance) within the marsupial forelimb skeleton, and lower integration between marsupial fore- and hind limbs, compared to other mammals. Possible mechanisms for this constraint are a fundamental developmental change in marsupial limb patterning, or alternatively more immediate perinatal biomechanical and metabolic requirements. In the latter case, peramelid marsupials (bandicoots), which have neonates that climb very little, should show lower within-limb and higher between-limb integration, compared to other marsupials. We tested this in four peramelid species and the related bilby, using partial correlation analyses of between-landmark linear measurements of limb bones, and Procrustes-based two-block partial least-squares analysis (2B-PLS) of limb bone shapes using the same landmarks. We find extensive between-limb integration in partial correlation analyses of only bone lengths, consistent with a reduction of a short-term biomechanical/allocation constraint in peramelid forelimbs. However, partial correlations of bone proportions and 2B-PLS reveal extensive shape divergence between correlated bone pairs. This result contradicts expectations of developmental constraints or serial homology, instead suggesting a function-driven integration pattern. Comparing visualizations from cross-species principal components analysis and 2BPLS, we tentatively identify selection for digging and halfbounding as the main driver of bandicoot limb integration patterning. This calls for further assessments of functional versus developmental limb integration in marsupials with a more strenuous neonatal climb to the pouch.V. Weisbecker was supported by Discovery Early Career Award (DE120102034) and a Discovery Grant (DP170103227) of the Australian Research Council, A. Marcy by the Australian-American Fulbright Commission (2014 U.S. Postgraduate Fulbright Scholarship)

Resolving the evolution of the mammalian middle ear using Bayesian inference

Background The minute, finely-tuned ear ossicles of mammals arose through a spectacular evolutionary transformation from their origins as a load-bearing jaw joint. This involved detachment from the postdentary trough of the mandible, and final separation from the dentary through resorption of Meckel’s cartilage. Recent parsimony analyses of modern and fossil mammals imply up to seven independent postdentary trough losses or even reversals, which is unexpected given the complexity of these transformations. Here we employ the first model-based, probabilistic analysis of the evolution of the definitive mammalian middle ear, supported by virtual 3D erosion simulations to assess for potential fossil preservation artifacts. Results Our results support a simple, biologically plausible scenario without reversals. The middle ear bones detach from the postdentary trough only twice among mammals, once each in the ancestors of therians and monotremes. Disappearance of Meckel’s cartilage occurred independently in numerous lineages from the Late Jurassic to the Late Cretaceous. This final separation is recapitulated during early development of extant mammals, while the earlier-occurring disappearance of a postdentary trough is not. Conclusions Our results therefore suggest a developmentally congruent and directional two-step scenario, in which the parallel uncoupling of the auditory and feeding systems in northern and southern hemisphere mammals underpinned further specialization in both lineages. Until ~168 Ma, all known mammals retained attached middle ear bones, yet all groups that diversified from ~163 Ma onwards had lost the postdentary trough, emphasizing the adaptive significance of this transformation

Developmental asynchrony and antagonism of sex determination pathways in a lizard with temperature-induced sex reversal

Abstract Vertebrate sex differentiation follows a conserved suite of developmental events: the bipotential gonads differentiate and shortly thereafter sex specific traits become dimorphic. However, this may not apply to squamates, a diverse vertebrate lineage comprising of many species with thermosensitive sexual development. Of the three species with data on the relative timing of gonad differentiation and genital dimorphism, the females of two (Niveoscincus ocellatus and Barisia imbricata) exhibit a phase of temporary pseudohermaphroditism or TPH (gonads have differentiated well before genital dimorphism). We report a third example of TPH in Pogona vitticeps, an agamid with temperature-induced male to female sex reversal. These findings suggest that for female squamates, genital and gonad development may not be closely synchronised, so that TPH may be common. We further observed a high frequency of ovotestes, a usually rare gonadal phenotype characterised by a mix of male and female structures, exclusively associated with temperature-induced sex reversal. We propose that ovotestes are evidence of a period of antagonism between male and female sex-determining pathways during sex reversal. Female sexual development in squamates is considerably more complex than has been appreciated, providing numerous avenues for future exploration of the genetic and hormonal cues that govern sexual development

Bats that walk: a new evolutionary hypothesis for the terrestrial behaviour of New Zealand's endemic mystacinids.

RIGHTS : This article is licensed under the BioMed Central licence at http://www.biomedcentral.com/about/license which is similar to the 'Creative Commons Attribution Licence'. In brief you may : copy, distribute, and display the work; make derivative works; or make commercial use of the work - under the following conditions: the original author must be given credit; for any reuse or distribution, it must be made clear to others what the license terms of this work are.BACKGROUND: New Zealand's lesser short-tailed bat Mystacina tuberculata is one of only two of c.1100 extant bat species to use a true walking gait when manoeuvring on the ground (the other being the American common vampire bat Desmodus rotundus). Mystacina tuberculata is also the last surviving member of Mystacinidae, the only mammalian family endemic to New Zealand (NZ) and a member of the Gondwanan bat superfamily Noctilionoidea. The capacity for true quadrupedal terrestrial locomotion in Mystacina is a secondarily derived condition, reflected in numerous skeletal and muscular specializations absent in other extant bats. The lack of ground-based predatory native NZ mammals has been assumed to have facilitated the evolution of terrestrial locomotion and the unique burrowing behaviour of Mystacina, just as flightlessness has arisen independently many times in island birds. New postcranial remains of an early Miocene mystacinid from continental Australia, Icarops aenae, offer an opportunity to test this hypothesis. RESULTS: Several distinctive derived features of the distal humerus are shared by the extant Mystacina tuberculata and the early Miocene Australian mystacinid Icarops aenae. Study of the myology of M. tuberculata indicates that these features are functionally correlated with terrestrial locomotion in this bat. Their presence in I. aenae suggests that this extinct mystacinid was also adapted for terrestrial locomotion, despite the existence of numerous ground-based mammalian predators in Australia during the early Miocene. Thus, it appears that mystacinids were already terrestrially-adapted prior to their isolation in NZ. In combination with recent molecular divergence dates, the new postcranial material of I. aenae constrains the timing of the evolution of terrestrial locomotion in mystacinids to between 51 and 26 million years ago (Ma). CONCLUSION: Contrary to existing hypotheses, our data suggest that bats are not overwhelmingly absent from the ground because of competition from, or predation by, other mammals. Rather, selective advantage appears to be the primary evolutionary driving force behind habitual terrestriality in the rare bats that walk. Unlike for birds, there is currently no evidence that any bat has evolved a reduced capacity for flight as a result of isolation on islands

Individual variation of the masticatory system dominates 3D skull shape in the herbivory-adapted marsupial wombats

BackgroundWithin-species skull shape variation of marsupial mammals is widely considered low and strongly size-dependent (allometric), possibly due to developmental constraints arising from the altricial birth of marsupials. However, species whose skulls are impacted by strong muscular stresses - particularly those produced through mastication of tough food items - may not display such intrinsic patterns very clearly because of the known plastic response of bone to muscle activity of the individual. In such cases, allometry may not dominate within-species shape variation, even if it is a driver of evolutionary shape divergence; ordination of shape in a geometric morphometric context through principal component analysis (PCA) should reveal main variation in areas under masticatory stress (incisor region/zygomatic arches/mandibular ramus); but this main variation should emerge from high individual variability and thus have low eigenvalues.ResultsWe assessed the evidence for high individual variation through 3D geometric morphometric shape analysis of crania and mandibles of three species of grazing-specialized wombats, whose diet of tough grasses puts considerable strain on their masticatory system. As expected, we found little allometry and low Principal Component 1 (PC1) eigenvalues within crania and mandibles of all three species. Also as expected, the main variation was in the muzzle, zygomatic arches, and masticatory muscle attachments of the mandibular ramus. We then implemented a new test to ask if the landmark variation reflected on PC1 was reflected in individuals with opposite PC1 scores and with opposite shapes in Procrustes space. This showed that correspondence between individual and ordinated shape variation was limited, indicating high levels of individual variability in the masticatory apparatus.DiscussionOur results are inconsistent with hypotheses that skull shape variation within marsupial species reflects a constraint pattern. Rather, they support suggestions that individual plasticity can be an important determinant of within-species shape variation in marsupials (and possibly other mammals) with high masticatory stresses, making it difficult to understand the degree to which intrinsic constraints act on shape variation at the within-species level. We conclude that studies that link micro- and macroevolutionary patterns of shape variation might benefit from a focus on species with low-impact mastication, such as carnivorous or frugivorous species

The Evolution of Fangs, Venom, and Mimicry Systems in Blenny Fishes

Venom systems have evolved on multiple occasions across the animal kingdom, and they can act as key adaptations to protect animals from predators. Consequently, venomous animals serve as models for a rich source of mimicry types, as non-venomous species benefit from reductions in predation risk by mimicking the coloration, body shape, and/or movement of toxic counterparts. The frequent evolution of such deceitful imitations provides notable examples of phenotypic convergence and are often invoked as classic exemplars of evolution by natural selection. Here, we investigate the evolution of fangs, venom, and mimetic relationships in reef fishes from the tribe Nemophini (fangblennies). Comparative morphological analyses reveal that enlarged canine teeth (fangs) originated at the base of the Nemophini radiation and have enabled a micropredatory feeding strategy in non-venomous Plagiotremus spp. Subsequently, the evolution of deep anterior grooves and their coupling to venom secretory tissue provide Meiacanthus spp. with toxic venom that they effectively employ for defense. We find that fangblenny venom contains a number of toxic components that have been independently recruited into other animal venoms, some of which cause toxicity via interactions with opioid receptors, and result in a multifunctional biochemical phenotype that exerts potent hypotensive effects. The evolution of fangblenny venom has seemingly led to phenotypic convergence via the formation of a diverse array of mimetic relationships that provide protective (Batesian mimicry) and predatory (aggressive mimicry) benefits to other fishes. Our results further our understanding of how novel morphological and biochemical adaptations stimulate ecological interactions in the natural world