Functional morphology of the bovid astragalus in relation to habitat: Controlling phylogenetic signal in ecomorphology

Bovid astragali are one of the most commonly preserved bones in the fossil record. Accordingly, astragali are an important target for studies seeking to predict the habitat preferences of fossil bovids based on bony anatomy. However, previous work has not tested functional hypotheses linking astragalar morphology with habitat while controlling for body size and phylogenetic signal. This article presents a functional framework relating the morphology of the bovid astragalus to habitat‐specific locomotor ecology and tests four hypotheses emanating from this framework. Highly cursorial bovids living in structurally open habitats are hypothesized to differ from their less cursorial closed‐habitat dwelling relatives in having (1) relatively short astragali to maintain rotational speed throughout the camming motion of the rotating astragalus, (2) a greater range of angular excursion at the hock, (3) relatively larger joint surface areas, and (4) a more pronounced “spline‐and‐groove” morphology promoting lateral joint stability. A diverse sample of 181 astragali from 50 extant species was scanned using a Next Engine laser scanner. Species were assigned to one of four habitat categories based on the published ecological literature. A series of 11 linear measurements and three joint surface areas were measured on each astragalus. A geometric mean body size proxy was used to size‐correct the measurement data. Phylogenetic generalized least squares (PGLS) was used to test for differences between habitat categories while controlling for body size differences and phylogenetic signal. Statistically significant PGLS results support Hypotheses 1 and 2 (which are not mutually exclusive) as well as Hypothesis 3. No support was found for Hypothesis 4. These findings confirm that the morphology of the bovid astragalus is related to habitat‐specific locomotor ecology, and that this relationship is statistically significant after controlling for body size and phylogeny. Thus, this study validates the use of this bone as an ecomorphological indicator. J. Morphol. 275:1201–1216, 2014. © 2014 Wiley Periodicals, Inc.     

Using functional traits and phylogeny to understand local extinction risk in dragonflies and damselflies (Odonata)

Understanding the risk of local extinction of a species is vital in conservation biology, especially now when anthropogenic disturbances and global warming are severely changing natural habitats. Local extinction risk depends on species traits, such as its geographical range size, fresh body mass, dispersal ability, length of flying period, life history variation, and how specialized it is regarding its breeding habitat. We used a phylogenetic approach because closely related species are not independent observations in the statistical tests. Our field data contained the local extinction risk of 31 odonate (dragonflies and damselflies) species from Central Finland. Species relatedness (i.e., phylogenetic signal) did not affect local extinction risk, length of flying period, nor the geographical range size of a species. However, we found that closely related species were similar in hind wing length, length of larval period, and habitat of larvae. Both phylogenetically corrected (PGLS) and uncorrected (GLM) analysis indicated that the geographical range size of species was negatively related to local extinction risk. Contrary to expectations, habitat specialist species did not have higher local extinction rates than habitat generalist species nor was it affected by the relatedness of species. As predicted, species’ long larval period increased, and long wings decreased the local extinction risk when evolutionary relatedness was controlled. Our results suggest that a relatively narrow geographical range size is an accurate estimate for a local extinction risk of an odonate species, but the species with long life history and large habitat niche width of adults increased local extinction risk. Because the results were so similar between PGLS and GLM methods, it seems that using a phylogenetic approach does not improve predicting local extinctions.     

Bovid postcranial ecomorphological survey of the Laetoli paleoenvironment

Here we report on a bovid postcranial ecomorphological survey of the fossil assemblages from the Plio-Pleistocene site of Laetoli, Tanzania. A global sample of extant bovids (n=205), cervids (n=14), and tragulids (n=5) from seven known habitat types constitutes the comparative data set. All long bones, carpals, tarsals, and phalanges were measured. Discriminant function analyses (DFA) were conducted in order to evaluate the ability of each element to accurately predict habitat affiliation. The baseline of chance accuracy for DFAs (i.e., the percentage of correct predictions that can be expected when habitat assignments are randomized) served as the cut-off point between good and bad habitat predictors. A total of 22 elements yielded percentages of correct classification over the baseline of accuracy, and these were extended to the Laetoli fossil assemblages. Summaries of the number of specimens predicted to belong to each habitat type were used to reconstruct the paleoenvironment. The results indicate that, at the time of the deposition of the Laetolil Beds, the area had heavy woodland-bushland cover with some lighter tree and bush cover and grass available. These results lend strong support to recent suggestions that the area was on the more wooded end of the habitat spectrum, contra initial conclusions that it represented a mosaic of more open habitats. The results also indicate that, during the deposition of the Ndolanya Beds, the environment had become more open and the grassland component of the environment had increased significantly. Light woodland-bushland and an abundance of grass cover dominated the landscape, although tracts of land with denser vegetation likely existed. This conclusion agrees with earlier suggestions that the area was a semiarid bushland.     

Dispersal is linked to habitat use in 59 species of water beetles (Coleoptera: Adephaga) on Madagascar

Lentic habitats (standing water, such as ponds and lakes) differ from lotic habitats (running water; streams and rivers) in their spatiotemporal persistence, with lentic habitats being more ephemeral in evolutionary time. This habitat instability is thought to select for dispersal, and several phylogenetic and macroecological studies have suggested that high rates of dispersal are more characteristic of lentic than lotic species. We tested this hypothesis using a comparative population genetic and phylogeographic approach based on mitochondrial DNA for 59 aquatic beetle species, sampled across Madagascar. Species were classified as lotic (n = 25), lentic (n = 25), or lotolentic (associated with both running and standing water; n = 9). Hierarchical population genetic structure (AMOVA), nucleotide diversity (π), and geographic structure were compared among habitat types. Lotic species had significantly greater population structure (Ф_ST = 0.55, hierarchical AMOVA) than lentic (Ф_ST = 0.13) and lotolentic (Ф_ST = 0.19) species using phylogenetic generalized least squares (PGLS) to correct for phylogeny. Body size was independent of habitat preference, and did not explain any of the intraspecific variation. A greater proportion of lotic species were endemic to Madagascar and lotic species had more pronounced geographic structure in their haplotype networks. The results indicate that dispersal is consistently lower among lotic species, independent of phylogenetic relatedness. This has macroevolutionary and biogeographical consequences for the freshwater fauna of this tropical biodiversity hotspot where remaining natural habitats are becoming increasingly isolated from one another.     

Exploring morphological evolution in relation to habitat moisture in the moss genus Fissidens using molecular data generated from herbarium specimens

Morphological evolution in mosses has long been hypothesized to accompany shifts in microhabitats, which can be tested using comparative phylogenetics. These lines of inquiry have been developed to include target capture sequencing, which can yield phylogenomic scale data from herbarium specimens. Here, we test the relationship between taxonomically important morphological characters in the moss genus Fissidens, using a 400-locus data set generated using a target-capture approach in tandem with a three-locus phylogeny generated using Sanger sequencing. Phylogenetic trees generated using ASTRAL and Bayesian inference were used to test the monophyly of subgenera/sections. These trees provide the basis for ancestral character state reconstructions and phylogenetic correlation analyses for five morphological characters and characters related to the moisture habitat, scored from the literature and by specimen inspection. Many of these characters exhibit statistically significant phylogenetic signal. Significant correlations were found between the limbidium (phyllid/leaf border of the gametophyte) and habitat moisture niche breadth, which could be interpreted as the more extensive limbidium enabling species to survive across a wider variety of habitats. We also found correlations between costa anatomy, peristome morphology, and the limbidium, which could reflect the evolutionary recruitment of genetic networks from the gametophyte to the sporophyte phase. The correlation found between average habitat moisture and the sexual system indicates that dioicous and polyoicous species are more likely to be found in moist habitats and that these higher moisture levels could be particularly, reproductively advantageous to species with separate sexes.     

Habitat choice in Phylloscopus warblers: the role of morphology, phylogeny and competition

We studied ecological and evolutionary aspects of habitat choice in a group of closely related bird species to gain insight into factors influencing bird community structure. Seven species of Phylloscopus warblers breed sympatrically in the middle taiga subzone of Central Siberia. We examine how the distribution of species among habitats is related to morphology, phylogeny and competition, and we compare our results with an earlier study on the ecomorphology of Phylloscopus warblers in Kashmir. We found that in Siberia, large warbler species prefer productive habitats with mostly deciduous vegetation, whereas small species occupy poor coniferous forests. Possible explanations for this finding remain to be tested in the future. Moreover, we found a tendency for species with large feet, small bills and short wings to occupy habitats with an abundance of bush thickets near the ground. In the Kashmir study, competition was considered a major factor in structuring the Phylloscopus community, and patterns of habitat choice were not influenced by phylogenetic relationships. In strong contrast, we found that in the Siberian community, closely related species occupy similar habitats. We discuss whether this conservative evolution of habitat preferences in Siberia may be due to low intensity of interspecific competition or to other ecological factors.     

Phylogenetic systematics and biomecha cs in ecomorphology

Synopsis Research in all fields of biology increasingly uses phylogenetic systematics to interpret biological data in an evolutionary context. It is becoming widely accepted that comparative studies of the correlation of biological features, such as ecomorphological studies, must frame their analyses within the context of a phylogenetic hierarchy rather than treating each taxonomic unit as an independent replicate. Recent methods for the interpretation of ecological and functional data in the framework of a phylogeny can reveal the degree to which ecomorphological characters are correlated with one another, and are congruent with hierarchical cladistic groups. An example of the ecomorphology of labrid fishes is used here to illustrate the application of several of these methods. The structural design and mechanics of the jaws of labrids are tested for ecomorphological associations with the natural diets of these fishes. Methods for analysis of the correlated evolution of both discrete and continuous quantitative characters within a phylogeny are practiced on a single ecomorphological data set. Techniques used include character coding, character mapping, phylogenetic autocorrelation, independent contrasts, and squared change parsimony. These approaches to diverse biological data allow the study of ecomorphology to account for patterns of phylogenetic ancestry. Biomechanics or functional morphology also plays a vital role in the determination of ecomorphological relationships by clarifying the mechanisms by which morphologies can perform behaviors important to the organism's ecology. The synthesis of systematics with biomechanics is an example of interdisciplinary study in which information exchange can elucidate patterns of evolution in ecomorphology.     

A statistical approach to the evaluation of characters to estimate evolutionary relationships among the species of the aquatic subterranean genus, Iberobathynella (Crustacea, Syncarida)

The 13 known species of the genus Iberobathynella were studied. Twenty-six characters with usually two or three states were revealed to have low within-species variability but show clear differences among some species. These characters were hypothesized to have states convex on the branching pattern of the phylogenetic lines that gave rise to these 13 species (i.e. be uniquely derived). Each pair of these hypotheses was tested for logical compatibility; then, for each character, a new character was created by choosing equiprobably one of the possible permutations of the 13 species to rename the species in each state. Characters created in this random way would have convex states only by chance, not by evolution. This random character was tested with each of the remaining 25 for logical compatibility as hypotheses of convexity. For each character, one thousand such random characters were created and tested. Sixteen observed characters were compatible with more other observed characters than 90% of their randomly generated counterparts, and so were considered plausibly non-random. They were used to speculate on branching patterns of the phylogenetic lines among the 13 species.     

Using Corine Land Cover Habitat Database for the analysis of breeding bird habitat: case study of white storks (Ciconia ciconia) from northern Croatia

The purpose of this study was to find out whether a set of habitat characteristics, derived from the National Corine Land Cover (CLC) database of habitat types, could indicate the occurrence of white stork nests in a settlement. The analyses were performed for the settlements closer than 35 km from the Drava River (northern Croatia). Sixteen habitat characteristics were determined around 257 settlements occupied with white stork nests and 152 control sites without white stork nests within the same geographic region. We performed multivariate inspection of the data and a non-metric multidimensional preference analysis. The best variables for stork habitat selection were: distance to the nearest grassland habitat (P < 0.0001), distance to three nearest grassland habitats (P < 0.0001), altitude of the settlements above the sea level (P < 0.001), sum of distances to the three nearest agricultural mosaic habitats (P < 0.005) and standardized area proportion of forests (P < 0.05). The explanatory capacity of the model was 81.1%. We conclude that it is possible to define a small number of habitat characteristics derived from CLC database which can indicate the occurrence of white stork nests.     

Phenotypic characters of static homology increase phylogenetic stability under direct optimization of otherwise dynamic homology characters

Direct optimization of unaligned sequence characters provides a natural framework to explore the sensitivity of phylogenetic hypotheses to variation in analytical parameters. Phenotypic data, when combined into such analyses, are typically analyzed with static homology correspondences unlike the dynamic homology sequence data. Static homology characters may be expected to constrain the direct optimization and thus, potentially increase the similarity of phylogenetic hypotheses under different cost sets. However, whether a total-evidence approach increases the phylogenetic stability or not remains empirically largely unexplored. Here, I studied the impact of static homology data on sensitivity using six empirical data sets composed of several molecular markers and phenotypic data. The inclusion of static homology phenotypic data increased the average stability of phylogenetic hypothesis in five out of the six data sets. To investigate if any static homology characters would have similar effect, the analyses were repeated with randomized phenotypic data, and with one of the molecular markers fixed as static homology characters. These analyses had, on average, almost no effect on the phylogenetic stability, although the randomized phenotypic data sometimes resulted in even higher stability than empirical phenotypic data. The impact was related to the strength of the phylogenetic signal in the phenotypic data: higher average jackknife support of the phenotypic tree correlated with stronger stabilizing effect in the total-evidence analysis. Phenotypic data with a strong signal made the total-evidence trees topologically more similar to the phenotypic trees, thus, they constrained the dynamic homology correspondences of the sequence data. Characters that increase phylogenetic stability are particularly valuable for phylogenetic inference. These results indicate an important role and additive value of phenotypic data in increasing the stability of phylogenetic hypotheses in total-evidence analyses.     

Colonization of a novel depauperate habitat leads to trophic niche shifts in three desert lizard species

In a novel, depauperate ecosystem, colonizing species may experience changes in their trophic niche as a result of a new resource base and fewer competitors and predators. To examine trophic niche shifts of recent colonists, we focused on three ecologically and phylogenetically divergent lizard species that inhabit both the geologically distinctive depauperate habitat of White Sands and the surrounding Chihuahuan ‘dark soil’ desert in New Mexico. In White Sands the three species comprise the entire lizard community, whereas in the dark soils habitat, they constitute less than half of the lizard community abundance. As a result, we hypothesized that the three focal species would collectively represent a greater variety of trophic positions in the White Sands habitat than in the dark soils habitat. We hypothesized that the extent of shifts in each species’ trophic position would parallel diet and ecomorphology differences between habitats. To test these hypotheses, we combined analysis of lizard stomach contents with carbon and nitrogen stable isotopes in the context of previously published ecomorphology measurements. Stable isotope data indicated that as predicted, species were more different from one another in White Sands than in dark soils, suggesting community‐wide ecological release. Overall, all species were lower on the White Sands food chain; however, only one species decreased trophic level significantly, one increased trophic level variance, and one did not change significantly. Furthermore, stomach content data paralleled both stable isotope and ecomorphological data, showing different degrees of dietary overlap between habitats, depending on the species. That species’ differences in trophic ecology also correspond with ecomorphological differences suggests that these factors are either causally linked or collectively responding to similar ecological pressures, such as competition. By examining diet, trophic position, and ecomorphology of three colonist species, we demonstrate both species‐specific and community‐wide trophic differences in adjacent, but distinct habitats.     

The robustness of a network of ecological networks to habitat loss

There have been considerable advances in our understanding of the tolerance of species interaction networks to sequential extinctions of plants and animals. However, communities of species exist in a mosaic of habitats, and the vulnerability of habitats to anthropogenic change varies. Here, we model the cascading effects of habitat loss, driven by plant extinctions, on the robustness of multiple animal groups. Our network is constructed from empirical observations of 11 animal groups in 12 habitats on farmland. We simulated sequential habitat removal scenarios: randomly; according to prior information; and with a genetic algorithm to identify best‐ and worst‐case permutations of habitat loss. We identified two semi‐natural habitats (waste ground and hedgerows together comprising < 5% of the total area of the farm) as disproportionately important to the integrity of the overall network. Our approach provides a new tool for network ecologists and for directing the management and restoration of multiple‐habitat sites.     

Selection of indicative taxa for river habitats: a case study on benthic macroinvertebrates using indicator species analysis and the random forest methods

The aim of the study was to evaluate the exclusivity and/or preference of macroinvertebrate taxa for river habitats. Indicator species analysis and random forests methods were applied to the data set of macroinvertebrate samples taken from 58 sampling points. Samples were classified according to habitat types defined by the position in a river channel and local hydraulic characteristics. 86 macroinvertebrate taxa were included in the analyses. High indicative values for habitats (importance value ≥50 and/or indicator value ≥40) were identified for 26 taxa. The results of both methods can be considered similar. Merged habitats of channel margin (margin of main channel and side arms) were mainly defined by “negative” indicator taxa (correct classification of given samples was caused by non-occurrence and low abundances of certain taxa in this habitat). In general, there was only a small group of taxa preferring these habitats. Taxa were not fully habitat specific because they mostly occurred in two or three habitat types. This could be the result of autecological plasticity of individual taxa and the connectivity among habitats. According to the experience from this case study, it can be concluded that both random forests and IndVal methods are suitable for the detection of indicative species, and random forests method has some additional advantages.     

Cross-sectional geometry of the dentary in bats

Bats exhibit remarkable diversity in dietary habits, with species specializing on insects, fruit, nectar, vertebrates and blood. Studies of larger mammals have shown that structural differences in dentary cross-sectional properties exist among species with different diets. Unfortunately, few of these studies have considered the role of phylogeny in shaping these apparent form-function associations. Here we ask whether a relationship exists between diet and dentary structure in bats when phylogenetic history is factored into the analysis. To answer this question, we compared results from phylogenetic generalized least squares (PGLS) and traditional (nonphylogenetic) regression analyses of dentary cross-sectional shape in frugivorous, nectarivorous, and insectivorous bats (253 individuals representing 72 species). Cross-sectional moments of inertia of the dentary between M(1) and M(2) were computed from bone densitometry scans of skeletal specimens. Traditional regressions of cross-sectional parameters against dentary length detected significant departures from isometry among frugivores. In contrast, PGLS analyses indicated that cross-sectional variables for each dietary group scaled with isometry. Thus, the allometric patterns illuminated by traditional statistics are linked to the phylogenetic structure of the sample. Identical patterns of significant differences in slopes and intercepts between frugivores and nectarivores emerged from both traditional and PGLS analyses. As predicted, the cross-sectional shape of the dentary in frugivores is consistent with increased resistance to torsion and bending, while that of nectarivores suggested a less resistant dentary. Although traditional and PGLS analyses yielded some similar results, the phylogenetic structure of a sample can drive apparent patterns of scaling and should be considered in comparative functional analyses.     

Size,relative abundance,and catch‐per‐unit‐effort of round goby,Neogobius melanostomus,in anthropogenically modified and natural habitats in the western basin of Lake Erie

To determine if anthropogenically modified habitats possess greater numbers of round goby and serve as dispersal vectors, we used angling to compare catch‐per‐unit of effort for 64 natural and modified habitat areas. In addition, a gravel natural habitat was seined to compare length frequency distribution with anthropogenically modified habitats. Natural habitats included gravel beaches and natural rubble and cliff wall, while modified habitats included artificial riprap, concrete sea wall, and metal sheet piling. No significant difference in relative abundance was observed in round goby preference among modified habitats (P = 0.52), but natural gravel habitats were significantly different from modified habitats that included artificial riprap (P = 0.002), concrete sea wall (P < 0.001), and metal sheet piling (P = 0.003). When habitat subcategories were compared using anova , the natural gravel beach habitat was significantly different from the three artificial substrates and from natural rubble and cliff wall substrates (P < 0.004). No round goby were caught from gravel beach habitats; thus, this habitat was removed from further analysis. A Student t‐test indicated no significant difference between habitats was found between the natural rubble and cliff wall habitat and the three other artificial habitats (concrete sea wall, P = 0.33; riprap, P = 0.53; metal sheet piling, P = 0.11). We further evaluated gravel beach habitats to determine the reason for the lack of goby capture. We seined gravel beach habitat and collected 328 individuals, with which we evaluated the length‐frequency distribution and calculated length–weight relationships by sex. Our results indicated that only 5.2% of the goby population was available for capture by angling on the gravel beach habitat. A t‐test comparing the demographic attributes between seining and angling indicated a significant difference between goby length (P < 0.001) and weight (P < 0.001). The regression slope indicated an ontogenetic habitat shift occurred near 62 mm standard length. Smaller round goby individuals were found in less structurally complex gravel beach habitat, while larger individuals were associated with complex habitat.     

Ribosomal RNA secondary structure: compensatory mutations and implications for phylogenetic analysis

Using sequence data from the 28S ribosomal RNA (rRNA) genes of selected vertebrates, we investigated the effects that constraints imposed by secondary structure have on the phylogenetic analysis of rRNA sequence data. Our analysis indicates that characters from both base-pairing regions (stems) and non-base-pairing regions (loops) contain phylogenetic information, as judged by the level of support of the phylogenetic results compared with a well-established tree based on both morphological and molecular data. The best results (the greatest level of support of well-accepted nodes) were obtained when the complete data set was used. However, some previously supported nodes were resolved using either the stem or loop bases alone. Stem bases sustain a greater number of compensatory mutations than would be expected at random, but the number is < 40% of that expected under a hypothesis of perfect compensation to maintain secondary structure. Therefore, we suggest that in phylogenetic analyses, the weighting of stem characters be reduced by no more than 20%, relative to that of loop characters. In contrast to previous suggestions, we do not recommend weighting of stem positions by one-half, compared with that of loop positions, because this overcompensates for the constraints that selection imposes on the secondary structure of rRNA.      

Phylogenetic habitat filtering influences forest nucleation in grasslands

Because species–environment interactions are mediated by phenotypic tradeoffs, the maintenance of ancestral traits in some phylogenetic clades and the emergence of evolutionary novelties in others are likely to limit the types of habitats that species occupy, generating phylogenetic habitat filtering. To test for phylogenetic habitat filtering in woody sapling communities in vegetation patches scattered in southern Brazilian grasslands, I estimated if patches of different sizes encompassed species of different phylogenetic groups. I analyzed patch composition with principal coordinates of phylogenetic structure (PCPS), extracted from a matrix of phylogeny‐weighted species composition, and compared these results against net relatedness index (NRI) analyses. NRI analysis revealed that most communities were phylogenetically random, and that patches of different sizes did not differ from each other with respect to NRI. The first four PCPS contained ? 91% of total variation in phylogeny‐weighted species composition. In the first two PCPS, scores of large patches differed from those of small and medium patches, which did not differ from each other. Large patches were associated with basal plant clades, whereas small patches were mostly related to asterids, and medium patches were phylogenetically diverse. Phylogenetic habitat filtering was detected only by PCPS analysis, possibly because NRI analysis does not take into account the habitat specificity of species. Taking phylogenetic habitat filtering into account in comparative studies likely enhances our capability to understand the ways that plants interact with their environment.     

Habitat‐related seed germination traits in alpine habitats

Understanding the key aspects of plant regeneration from seeds is crucial in assessing species assembly to their habitats. However, the regenerative traits of seed dormancy and germination are underrepresented in this context. In the alpine zone, the large species and microhabitat diversity provide an ideal context to assess habitat‐related regenerative strategies. To this end, seeds of 53 species growing in alpine siliceous and calcareous habitats (6230 and 6170 of EU Directive 92/43, respectively) were exposed to different temperature treatments under controlled laboratory conditions. Germination strategies in each habitat were identified by clustering with k‐means. Then, phylogenetic least squares correlations (PGLS) were fitted to assess germination and dormancy differences between species’ main habitat (calcareous and siliceous), microhabitat (grasslands, heaths, rocky, and species with no specific microhabitats), and chorology (arctic–alpine and continental). Calcareous and siliceous grasslands significantly differ in their germination behaviour with a slow, mostly overwinter germination and high germination under all conditions, respectively. Species with high overwinter germination occurs mostly in heaths and have an arctic–alpine distribution. Meanwhile, species with low or high germinability in general inhabit in grasslands or have no specific microhabitat (they belong to generalist), respectively. Alpine species use different germination strategies depending on habitat provenance, species’ main microhabitat, and chorotype. Such differences may reflect adaptations to local environmental conditions and highlight the functional role of germination and dormancy in community ecology.