Periodic Environmental Disturbance Drives Repeated Ecomorphological Diversification in an Adaptive Radiation of Antarctic Fishes.

AbstractThe ecological theory of adaptive radiation has profoundly shaped our conceptualization of the rules that govern diversification. However, while many radiations follow classic early-burst patterns of diversification as they fill ecological space, the longer-term fates of these radiations depend on many factors, such as climatic stability. In systems with periodic disturbances, species-rich clades can contain nested adaptive radiations of subclades with their own distinct diversification histories, and how adaptive radiation theory applies in these cases is less clear. Here, we investigated patterns of ecological and phenotypic diversification within two iterative adaptive radiations of cryonotothenioid fishes in Antarctica's Southern Ocean: crocodile icefishes and notoperches. For both clades, we observe evidence of repeated diversification into disparate regions of trait space between closely related taxa and into overlapping regions of trait space between distantly related taxa. We additionally find little evidence that patterns of ecological divergence are correlated with evolution of morphological disparity, suggesting that these axes of divergence may not be tightly linked. Finally, we reveal evidence of repeated convergence in sympatry that suggests niche complementarity. These findings reflect the dynamic history of Antarctic marine habitats and may guide hypotheses of diversification dynamics in environments characterized by periodic disturbance.

Anthropogenic pressures drive population genetic structuring across a Critically Endangered lemur species range.

In recent decades Madagascar has experienced significant habitat loss and modification, with minimal understanding of how human land use practices have impacted the evolution of its flora and fauna. In light of ongoing and intensifying anthropogenic pressures, we seek new insight into mechanisms driving genetic variability on this island, using a Critically Endangered lemur species, the black-and-white ruffed lemur (Varecia variegata), as a test case. Here, we examine the relative influence of natural and anthropogenic landscape features that we predict will impose barriers to dispersal and promote genetic structuring across the species range. Using circuit theory, we model functional connectivity among 18 sampling localities using population-based genetic distance (FST). We optimized resistance surfaces using genetic algorithms and assessed their performance using maximum-likelihood population-effects mixed models. The best supported resistance model was a composite surface that included two anthropogenic features, habitat cover and distance to villages, suggesting that rapid land cover modification by humans has driven change in the genetic structure of wild lemurs. Primary conservation priority should be placed on mitigating further forest loss and connecting regions identified as having low dispersal potential to prevent further loss of genetic diversity and promote the survival of other moist forest specialists.

Reconciling species diversity in a tropical plant clade (Canarium, Burseraceae).

The challenges associated with sampling rare species or populations can limit our ability to make accurate and informed estimates of biodiversity for clades or ecosystems. This may be particularly true for tropical trees, which tend to be poorly sampled, and are thought to harbor extensive cryptic diversity. Here, we integrate genomics, morphology, and geography to estimate the number of species in a clade of dioecious tropical trees (Canarium L.; Burseraceae) endemic to Madagascar, for which previous taxonomic treatments have recognized between one and 33 species. By sampling genomic data from even a limited number of individuals per taxon, we were able to clearly reject both previous hypotheses, and support instead an intermediate number of taxa. We recognize at least six distinct clades based on genetic structure and species delimitation analyses that correspond clearly with geographic and discrete morphological differences. Two widespread clades co-occur broadly throughout eastern wet forests, one clade is endemic to western dry forests, and several slightly admixed clades are more narrowly distributed in mountainous regions in the north. Multiple previously described taxa were recovered as paraphyletic in our analyses, some of which were associated with admixed individuals, suggesting that hybridization contributes to taxonomic difficulties in Canarium. An improved understanding of Canarium species diversity has important implications for conservation efforts and understanding the origins of diversity in Madagascar. Our study shows that even limited genomic sampling, when combined with geography and morphology, can greatly improve estimates of species diversity for difficult tropical clades.

Cradles and museums of Antarctic teleost biodiversity.

Isolated in one of the most extreme marine environments on Earth, teleost fish diversity in Antarctica's Southern Ocean is dominated by one lineage: the notothenioids. Throughout the past century, the long-term persistence of this unique marine fauna has become increasingly threatened by regional atmospheric and, to a lesser extent oceanic, warming. Developing an understanding of how historical temperature shifts have shaped source-sink dynamics for Antarctica's teleost lineages provides critical insight for predicting future demographic responses to climate change. We use a combination of phylogenetic and biogeographic modelling to show that high-latitude Antarctic nearshore habitats have been an evolutionary sink for notothenioid species diversity. Contrary to expectations from island biogeographic theory, lower latitude regions of the Southern Ocean that include the northern Antarctic Peninsula and peripheral island archipelagos act as source areas to continental diversity. These peripheral areas facilitate both the generation of new species and repeated colonization of nearshore Antarctic continental regions. Our results provide historical context to contemporary trends of global climate change that threaten to invert these evolutionary dynamics.

The Paucity of Frugivores in Madagascar May Not Be Due to Unpredictable Temperatures or Fruit Resources.

The evolution of ecological idiosyncrasies in Madagascar has often been attributed to selective pressures stemming from extreme unpredictability in climate and resource availability compared to other tropical areas. With the exception of rainfall, few studies have investigated these assumptions. To assess the hypothesis that Madagascar's paucity of frugivores is due to unreliability in fruiting resources, we use statistical modeling to analyze phenology datasets and their environmental correlates from two tropical wet forests, the Réserve Naturelle Intégrale Betampona in Madagascar, and Kibale National Park in Uganda. At each site we found that temperature is a good environmental predictor of fruit availability. We found no evidence of a significant difference in the predictability of fruit availability between the two sites, although the shorter duration of phenological monitoring at Betampona (two years, versus 15 years at Kibale) limits our ability to infer long-term patterns. Comparisons of long-term temperature data from each site (15 years from Kibale and 14 from Betampona) indicate that temperature is more predictable at Betampona than at Kibale. However, there does appear to be a difference between the two sites in the total fruit availability at any given time, with fruit being generally less abundant at Betampona. Our results appear contrary to the prevailing hypothesis of a selective force imposed by unpredictable resource availability or temperature, and we suggest other possible explanations for Madagascar's unique biota.

Cryptic species diversity in sub-Antarctic islands: A case study of Lepidonotothen.

The marine fauna of the Southern Ocean is well known for an impressive adaptive radiation of fishes, the notothenioids. However, when compared to other marine areas, the frigid waters of the Southern Ocean also contain a seemingly large proportion of cryptic species. The documented instances of speciation in the absence of morphological change are largely observed in invertebrate taxa, in particular around peri- and sub-Antarctic islands such as South Georgia, which has been dubbed a cryptic species hotspot. This prevalence of cryptic species raises the question of how generalizable these patterns are for Antarctic vertebrates. Here we examine aspects of genotype and phenotype in an Antarctic notothenioid fish species, Lepidonotothen nudifrons, which is distributed in near shore habitats of the Antarctic Peninsula, South Orkney Islands, South Georgia, and the South Sandwich Islands. The results of our analyses show that L. nudifrons comprises two species. We highlight that cryptic species are phenomena not restricted to invertebrate lineages, raising the possibility that the species diversity of notothenioids and other Southern Ocean fishes is under-described. In addition, our findings raise several questions about the evolutionary origin and maintenance of morphological stasis in one of the most extreme habitats on earth.

Implications of lemuriform extinctions for the Malagasy flora.

Madagascar's lemurs display a diverse array of feeding strategies with complex relationships to seed dispersal mechanisms in Malagasy plants. Although these relationships have been explored previously on a case-by-case basis, we present here the first comprehensive analysis of lemuriform feeding, to our knowledge, and its hypothesized effects on seed dispersal and the long-term survival of Malagasy plant lineages. We used a molecular phylogenetic framework to examine the mode and tempo of diet evolution, and to quantify the associated morphological space occupied by Madagascar's lemurs, both extinct and extant. Using statistical models and morphometric analyses, we demonstrate that the extinction of large-bodied lemurs resulted in a significant reduction in functional morphological space associated with seed dispersal ability. These reductions carry potentially far-reaching consequences for Malagasy ecosystems, and we highlight large-seeded Malagasy plants that appear to be without extant animal dispersers. We also identify living lemurs that are endangered yet occupy unique and essential dispersal niches defined by our morphometric analyses.

The biogeographic origin of a radiation of trees in Madagascar: implications for the assembly of a tropical forest biome.

BACKGROUND: Madagascar's rain forests are characterized by extreme and uneven patterns of species richness and endemicity, the biogeographic and evolutionary origins of which are poorly understood. METHODS: Here we use a time-calibrated phylogeny of a dominant group of trees in Madagascar's eastern rain forests, Canarium, and related Burseraceae (Canarieae), to test biogeographic hypotheses regarding the origin and radiation of the flora of this unique biome. RESULTS: Our findings strongly support the monophyly of Malagasy Canarium, suggesting that this clade represents a previously undocumented in situ radiation. Contrary to expectations of dispersal from Africa during the Oligocene, concurrent with the formation of Madagascar's rain forest biome, our analyses support a late Miocene origin for Malagasy Canarium, probably by long distance dispersal from Southeast Asia. DISCUSSION: Our study illustrates the importance of considering long distance dispersal as a viable explanation for clades with pantropical distributions diversifying subsequent to the Oligocene, and it highlights the formation of the Indo-Australian Archipelago and associated fast-moving equatorial surface currents, suggesting an under-appreciated evolutionary link among tropical centers of endemism. CONCLUSIONS: We postulate that the relatively recent establishment and radiation of Canarium in Madagascar may have been facilitated by the highly stochastic climates associated with these forest ecosystems.