Spatiotemporal patterns of avian host-parasite interactions in the face of biogeographical range expansions.

Exploration of interactions between hosts and parasitic symbionts is important for our understanding of the temporal and spatial distribution of organisms. For example, host colonization of new geographical regions may alter levels of infections and parasite specificity, and even allow hosts to escape from co-evolved parasites, consequently shaping spatial distributions and community structure of both host and parasite. Here we investigate the effect of host colonization of new regions and the elevational distribution of host-parasite associations between birds and their vector-transmitted haemosporidian blood parasites in two geological and geographical settings: mountains of New Guinea and the Canary Islands. Our results demonstrate that bird communities in younger regions have significantly lower levels of parasitism compared to those of older regions. Furthermore, host-parasite network analyses demonstrate that blood parasites may respond differently after arriving to a new region, through adaptations that allow for either expanding (Canary Islands) or retaining (New Guinea) their host niches. The spatial prevalence patterns along elevational gradients differed in the two regions, suggesting that region-specific biotic (e.g., host community) and abiotic factors (e.g., temperature) govern prevalence patterns. Our findings suggest that the spatiotemporal range dynamics in host-parasite systems are driven by multiple factors, but that host and parasite community compositions and colonization histories are of particular importance.

Sperm length variation among Afrotropical songbirds reflects phylogeny rather than adaptations to the tropical environment.

Sperm cells vary tremendously in size and shape across the animal kingdom. In songbirds (Aves: Passeri), sperm have a characteristic helical form but vary considerably in size. Most of our knowledge about sperm morphology in this group stems from studies of species in the Northern temperate zone, while little is known about the numerous species in the tropics. Here we examined sperm size in 125 Afrotropical songbird species with emphasis on the length of the major structural components (head, midpiece, flagellum), and total sperm length measured using light microscopy. Mean total sperm length varied from 51 µm to 212 µm across species. Those belonging to the Corvoidea superfamily had relatively short sperm with a small midpiece, while those of the three major Passeridan superfamilies Passeroidea, Muscicapoidea and Sylvioidea showed large interspecific variation in total sperm length and associated variation in midpiece length. These patterns are consistent with previous findings for temperate species in the same major clades. A comparative analysis with songbird species from the Northern temperate zone (N = 139) showed large overlap in sperm length ranges although certain temperate families (e.g. Parulidae, Emberizidae) typically have long sperm and certain Afrotropical families (e.g. Cisticolidae, Estrildidae) have relatively short sperm. Afrotropical and temperate species belonging to the same families showed no consistent contrasts in sperm length. Sperm length variation among Afrotropical and Northern temperate songbirds exhibits a strong phylogenetic signal with little or no evidence for any directional latitudinal effect among closely related taxa.

The association between morphological and ecological characters across a global passerine radiation.

Strong relationships between morphological and ecological characters are commonly predicted to reflect the association between form and function, with this hypothesis being well supported in restricted taxonomic and geographical contexts. Conversely, among broader sets of species, ecological variables have been shown to have limited power to explain morphological variation. To understand these apparent discrepancies, for a large and globally distributed passerine radiation, we test whether (a) the character states of four ecological variables (foraging mode, diet, strata and habitat) have different morphological optima, (b) ecological variables explain substantial variance in morphology and (c) ecological character states can be accurately predicted from morphology. We collected 10 linear morphological measurements for 782 species of corvoid passerines, and assessed (a) the fit of models of continuous trait evolution with different morphological optima for each ecological character state, (b) variation in morphological traits among ecological character states using phylogenetically corrected regressions and (c) the accuracy of morphological traits in predicting species-level membership of ecological character states using linear discriminant analysis (LDA). Models of morphological evolution with different ecological optima were well supported across numerous morphological axes, corresponding with significant differences in trait distributions among ecological character states. LDA also showed that membership of the ecological categories can be predicted with relatively high accuracy by morphology. In contrast to these findings, ecological variables explain limited amounts of variation in morphological traits. For a global radiation of passerine birds, we confirm that the generation of morphological variation is generally consistent with ecological selection pressures, but that ecological characters are of limited utility in explaining morphological differences among species. Although selection towards different optima means that membership of ecological character states tend to be well predicted by morphology, the overall morphospace of individual ecological character states tend to be broad, implying that morphology can evolve in multiple ways in response to similar selection pressures. Extensive variation in morphological adaptations among similar ecological strategies is likely to be a widespread phenomenon across the tree of life.

Evolution of female promiscuity in Passerides songbirds.

BACKGROUND: Female promiscuity is highly variable among birds, and particularly among songbirds. Comparative work has identified several patterns of covariation with social, sexual, ecological and life history traits. However, it is unclear whether these patterns reflect causes or consequences of female promiscuity, or if they are byproducts of some unknown evolutionary drivers. Moreover, factors that explain promiscuity at the deep nodes in the phylogenetic tree may be different from those important at the tips, i.e. among closely related species. Here we examine the relationships between female promiscuity and a broad set of predictor variables in a comprehensive data set (N = 202 species) of Passerides songbirds, which is a highly diversified infraorder of the Passeriformes exhibiting significant variation in female promiscuity. RESULTS: Female promiscuity was highly variable in all major clades of the Passerides phylogeny and also among closely related species. We found several significant associations with female promiscuity, albeit with fairly small effect sizes (all R2 ≤ 0.08). More promiscuous species had: 1) less male parental care, particularly during the early stages of the nesting cycle (nest building and incubation), 2) more short-term pair bonds, 3) greater degree of sexual dichromatism, primarily because females were drabber, 4) more migratory behaviour, and 5) stronger pre-mating sexual selection. In a multivariate model, however, the effect of sexual selection disappeared, while the other four variables showed additive effects and together explained about 16% of the total variance in female promiscuity. Female promiscuity showed no relationship with body size, life history variation, latitude or cooperative breeding. CONCLUSIONS: We found that multiple traits were associated with female promiscuity, but these associations were generally weak. Some traits, such as reduced parental care in males and more cryptic plumage in females, might even be responses to, rather than causes of, variation in female promiscuity. Hence, the high variation in female promiscuity among Passerides species remains enigmatic. Female promiscuity seems to be a rapidly evolving trait that often diverges between species with similar ecologies and breeding systems. A future challenge is therefore to understand what drives within-lineage variation in female promiscuity over microevolutionary time scales.

Adaptive radiation and the evolution of nectarivory in a large songbird clade.

The accumulation of exceptional ecological diversity within a lineage is a key feature of adaptive radiation resulting from diversification associated with the subdivision of previously underutilized resources. The invasion of unoccupied niche space is predicted to be a key determinant of adaptive diversification, and this process may be particularly important if the diversity of competing lineages within the area, in which the radiation unfolds, is already high. Here, we test whether the evolution of nectarivory resulted in significantly higher rates of morphological evolution, more extensive morphological disparity, and a heightened build-up of sympatric species diversity in a large adaptive radiation of passerine birds (the honeyeaters, about 190 species) that have diversified extensively throughout continental and insular settings. We find that a large increase in rates of body size evolution and general expansion in morphological space followed an ancestral shift to nectarivory, enabling the build-up of large numbers of co-occurring species that vary greatly in size, compared to related and co-distributed nonnectarivorous clades. These results strongly support the idea that evolutionary shifts into novel areas of niche space play a key role in promoting adaptive radiation in the presence of likely competing lineages.

Environmental determinism, and not interspecific competition, drives morphological variability in Australasian warblers (Acanthizidae).

Interspecific competition is thought to play a key role in determining the coexistence of closely related species within adaptive radiations. Competition for ecological resources can lead to different outcomes from character displacement to, ultimately, competitive exclusion. Accordingly, divergent natural selection should disfavor those species that are the most similar to their competitor in resource use, thereby increasing morphological disparity. Here, we examined ecomorphological variability within an Australo-Papuan bird radiation, the Acanthizidae, which include both allopatric and sympatric complexes. In addition, we investigated whether morphological similarities between species are related to environmental factors at fine scale (foraging niche) and/or large scale (climate). Contrary to that predicted by the competition hypothesis, we did not find a significant correlation between the morphological similarities found between species and their degree of range overlap. Comparative modeling based on both a priori and data-driven identification of selective regimes suggested that foraging niche is a poor predictor of morphological variability in acanthizids. By contrast, our results indicate that climatic conditions were an important factor in the formation of morphological variation. We found a significant negative correlation between species scores for PC1 (positively associated to tarsus length and tail length) and both temperature and precipitation, whereas PC2 (positively associated to bill length and wing length) correlated positively with precipitation. In addition, we found that species inhabiting the same region are closer to each other in morphospace than to species outside that region regardless of genus to which they belong or its foraging strategy. Our results indicate that the conservative body form of acanthizids is one that can work under a wide variety of environments (an all-purpose morphology), and the observed interspecific similarity is probably driven by the common response to environment.

Molecular phylogenetics and species limits in a cryptically coloured radiation of Australo-Papuan passerine birds (Pachycephalidae: Colluricincla).

Detailed knowledge of species limits is an essential component of the study of biodiversity. Although accurate species delimitation usually requires detailed knowledge of both genetic and phenotypic variation, such variation may be limited or unavailable for some groups. In this study, we reconstruct a molecular phylogeny for all currently recognized species and subspecies of Australasian shrikethrushes (Colluricincla), including the first sequences of the poorly known C. tenebrosa. Using a novel method for species delimitation, the multi-rate Poisson Tree Process (mPTP), in concordance with the phylogenetic data, we estimate species limits in this genetically diverse, but phenotypically subtly differentiated complex of birds. In line with previous studies, we find that one species, the little shrikethrush (C. megarhyncha) is characterized by deep divergences among populations. Delimitation results suggest that these clades represent distinct species and we consequently propose a new classification. Furthermore, our findings suggest that C. megarhyncha melanorhyncha of Biak Island does not belong in this genus, but is nested within the whistlers (Pachycephala) as sister to P. phaionota. This study represents a useful example of species delimitation when phenotypic variation is limited or poorly defined.

Expansion in geographical and morphological space drives continued lineage diversification in a global passerine radiation.

Why diversification rates vary so extensively across the tree of life remains an important yet unresolved issue in biology. Two prominent and potentially independent factors proposed to explain these trends reflect the capacity of lineages to expand into new areas of (i) geographical or (ii) ecological space. Here, we present the first global assessment of how diversification rates vary as a consequence of geographical and ecological expansion, studying these trends among 15 speciose passerine families (together approximately 750 species) using phylogenetic path analysis. We find that relative slowdowns in diversification rates characterize families that have accumulated large numbers of co-occurring species (at the 1° scale) within restricted geographical areas. Conversely, more constant diversification through time is prevalent among families in which species show limited range overlap. Relative co-occurrence is itself also a strong predictor of ecological divergence (here approximated by morphological divergence among species); however, once the relationship between co-occurrence and diversification rates have been accounted for, increased ecological divergence is an additional explanatory factor accounting for why some lineages continue to diversify towards the present. We conclude that opportunities for prolonged diversification are predominantly determined by continued geographical range expansion and to a lesser degree by ecological divergence among lineages.

Supermatrix phylogeny and biogeography of the Australasian Meliphagides radiation (Aves: Passeriformes).

With nearly 300 species, the infraorder Meliphagides represents one of the largest and most conspicuous Australasian bird radiations. Although the group has been the focus of a number of recent phylogenetic studies, a comprehensive species-level phylogenetic hypothesis is still lacking. This has impeded the assessment of broad-scale evolutionary, biogeographic and ecological hypotheses. In the present study, we use a supermatrix approach including five mitochondrial and four nuclear markers to infer a time-calibrated phylogeny of the Meliphagides. Our phylogeny, which includes 286 of the 289 (99%) currently recognized species, is largely congruent with previous estimates. However, the addition of 60 newly sequenced species reveals some novel relationships. Our biogeographic analyses suggest an Australian origin for the group in the early Oligocene (31.3Mya, 95% HPD 25.2-38.2Mya). In addition, we find that dispersal events out of Australia have been numerous and frequent, particularly to New Guinea, which has also been the source of multiple back-colonizations to the Australian mainland. The phylogeny provides an important framework for studying a wide variety of macroecological and macroevolutionary themes, including character evolution, origin and timing of diversification, biogeographic patterns and species responses to climate change.

The influence of wing morphology upon the dispersal, geographical distributions and diversification of the Corvides (Aves; Passeriformes).

New species are sometimes known to arise as a consequence of the dispersal and establishment of populations in new areas. It has nevertheless been difficult to demonstrate an empirical link between rates of dispersal and diversification, partly because dispersal abilities are challenging to quantify. Here, using wing morphology as a proxy for dispersal ability, we assess this relationship among the global radiation of corvoid birds. We found that species distributions are associated with wing shape. Widespread species (occurring on both islands and continents), and those that are migratory, exhibit wing morphologies better adapted to long-distance flight compared with sedentary continental or insular forms. Habitat preferences also strongly predict wing form, with species that occur in canopies and/or areas of sparse vegetation possessing dispersive morphologies. By contrast, we found no significant differences in diversification rates among either the migratory or habitat classifications, but species distributed in island settings diversify at higher rates than those found on continents. This latter finding may reflect the elevated dispersal capabilities of widespread taxa, facilitating the radiation of these lineages across insular areas. However, as the correlations between wing morphology and diversification rates were consistently weak throughout our dataset, this suggests that historical patterns of diversification are not particularly well reflected by present-day wing morphology.

Breeding system evolution influenced the geographic expansion and diversification of the core Corvoidea (Aves: Passeriformes).

Birds vary greatly in their life-history strategies, including their breeding systems, which range from brood parasitism to a system with multiple nonbreeding helpers at the nest. By far the most common arrangement, however, is where both parents participate in raising the young. The traits associated with parental care have been suggested to affect dispersal propensity and lineage diversification, but to date tests of this potential relationship at broad temporal and spatial scales have been limited. Here, using data from a globally distributed group of corvoid birds in concordance with state-dependent speciation and extinction models, we suggest that pair breeding is associated with elevated speciation rates. Estimates of transition between breeding systems imply that cooperative lineages frequently evolve biparental care, whereas pair breeders rarely become cooperative. We further highlight that these groups have differences in their spatial distributions, with pair breeders overrepresented on islands, and cooperative breeders mainly found on continents. Finally, we find that speciation rates appear to be significantly higher on islands compared to continents. These results imply that the transition from cooperative breeding to pair breeding was likely a significant contributing factor facilitating dispersal across tropical archipelagos, and subsequent world-wide phylogenetic expansion among the core Corvoidea.