Phylogeny of magpie‐robins and shamas (Aves: Turdidae: Copsychus and Trichixos): implications for island biogeography in Southeast Asia

Aim Magpie‐robins and shamas are forest and woodland birds of south Asia. There are two genera: Trichixos for the monotypic T. pyrrhopygus, and Copsychus for other species. Two species are widespread, whereas the others are restricted to specific islands. Endemicity is highest in the Philippines. Using phylogenetic methods, we examined how this group came to its unusual distribution. Location Mainland Asia from India to southern China, and islands from Madagascar to the Philippines. Particular emphasis is placed on the Greater Sundas and Philippines. Methods The phylogeny was estimated from DNA sequences of 14 ingroup taxa representing all nine currently recognized Copsychus and Trichixos species. The entire mitochondrial ND2 gene and portions of nuclear myoglobin intron 2 (Myo2) and transforming growth factor beta 2 intron 5 (TGFβ2‐5) were sequenced for all but two species. The phylogeny was reconstructed using maximum likelihood and Bayesian methods. The timing of divergence events was estimated using a relaxed molecular clock approach, and ancestral areas were examined using stochastic modelling. Results The group comprises three main clades corresponding to ecological types: Trichixos, a primary‐forest specialist; Copsychus magpie‐robins, open‐woodland and coastal species; and Copsychus shamas, thick‐forest species. Trichixos appears to be sister to the magpie‐robins, rendering Copsychus polyphyletic. The dating of phylogenetic nodes was too ambiguous to provide substantial insight into specific geographical events responsible for divergence within the group. Some patterns are nevertheless clear. Copsychus shamas reached the Philippines, probably in two separate invasions, and split into endemic species. Copsychus malabaricus and C. saularis expanded widely in the Greater Sundas and mainland Southeast Asia without species‐level diversification. Main conclusions Magpie‐robins are excellent dispersers and have diversified into distinct species only on isolated oceanic islands. Trichixos, a poor disperser, is restricted to mature forests of the Malay Peninsula, Sumatra and Borneo. Copsychus shamas are intermediate in habitat preference and dispersal capabilities. Their endemism in the Philippines may be attributed to early colonization and specialization to interior forests. In the Greater Sundas, C. malabaricus and C. saularis populations split and came together on Borneo to form two separate subspecies (of each species), which now hybridize.     

Dynamic colonization exchanges between continents and islands drive diversification in paradise‐flycatchers (Terpsiphone,Monarchidae)

Aim We use parametric biogeographical reconstruction based on an extensive DNA sequence dataset to characterize the spatio‐temporal pattern of colonization of the Old World monarch flycatchers (Monarchidae). We then use this framework to examine the role of dispersal and colonization in their evolutionary diversification and to compare plumages between island and continental Terpsiphone species. Location Africa, Asia and the Indian Ocean. Methods We generate a DNA sequence dataset of 2300 bp comprising one nuclear and three mitochondrial markers for 89% (17/19) of the Old World Monarchidae species and 70% of the Terpsiphone subspecies. By applying maximum likelihood and Bayesian phylogenetic methods and implementing a Bayesian molecular clock to provide a temporal framework, we reveal the evolutionary history of the group. Furthermore, we employ both Lagrange and Bayes‐ Lagrange analyses to assess ancestral areas at each node of the phylogeny. By combining the ancestral area reconstruction with information on plumage traits we are able to compare patterns of plumage evolution on islands and continents. Results We provide the first comprehensive molecular phylogenetic reconstruction for the Old World Monarchidae. Our phylogenetic results reveal a relatively recent diversification associated with several dispersal events within this group. Moreover, ancestral area analyses reveal an Asian origin of the Indian Ocean and African clades. Ancestral state reconstruction analyses of plumage characters provide an interpretation of the plumage differentiation on islands and continents. Ancestral plumage traits are inferred to be close to those of the Asian paradise‐flycatcher (Terpsiphone paradisi), and island species display a high degree of plumage autapomorphy compared with continental species. Main conclusions Terpsiphone paradisi is polyphyletic and comprises populations that have retained the ancestral plumage of the widespread Terpsiphone genus. The genus appears to have colonized south‐west Asia, the Indian Ocean and Africa from eastern Asia. The phylogeny and divergence time estimates indicate multiple simultaneous colonizations of the western Old World by Terpsiphone. These results reinforce a hypothesis of range expansions of a Terpsiphone paradisi‐like ancestor into eastern Asia and the western Old World.     

Vulnerability of terrestrial island vertebrates to projected sea‐level rise

Sea‐level rise (SLR) from global warming may have severe consequences for biodiversity; however, a baseline, broad‐scale assessment of the potential consequences of SLR for island biodiversity is lacking. Here, we quantify area loss for over 12 900 islands and over 3000 terrestrial vertebrates in the Pacific and Southeast Asia under three different SLR scenarios (1 m, 3 m and 6 m). We used very fine‐grained elevation information, which offered >100 times greater spatial detail than previous analyses and allowed us to evaluate thousands of hitherto not assessed small islands. Depending on the SLR scenario, we estimate that 15–62% of islands in our study region will be completely inundated and 19–24% will lose 50–99% of their area. Overall, we project that between 1% and 9% of the total island area in our study region may be lost. We find that Pacific species are 2–3 times more vulnerable than those in the Indomalayan or Australasian region and risk losing 4–22% of range area (1–6 m SLR). Species already listed as threatened by IUCN are particularly vulnerable compared with non‐threatened species. Under a simple area loss–species loss proportionality assumption, we estimate that 37 island group endemic species in this region risk complete inundation of their current global distribution in the 1 m SLR scenario that is widely anticipated for this century (and 118 species under 3 m SLR). Our analysis provides a first, broad‐scale estimate of the potential consequences of SLR for island biodiversity and our findings confirm that islands are extremely vulnerable to sea‐level rise even within this century.     

Niche divergence promotes rapid diversification of East African sky island white‐eyes (Aves: Zosteropidae)

The Eastern Afromontane biodiversity hotspot composed of highly fragmented forested highlands (sky islands) harbours exceptional diversity and endemicity, particularly within birds. To explain their elevated diversity within this region, models founded on niche conservatism have been offered, although detailed phylogeographic studies are limited to a few avian lineages. Here, we focus on the recent songbird genus Zosterops, represented by montane and lowland members, to test the roles of niche conservatism versus niche divergence in the diversification and colonization of East Africa's sky islands. The species‐rich white‐eyes are a typically homogeneous family with an exceptional colonizing ability, but in contrast to their diversity on oceanic islands, continental diversity is considered depauperate and has been largely neglected. Molecular phylogenetic analysis of ~140 taxa reveals extensive polyphyly among different montane populations of Z. poliogastrus. These larger endemic birds are shown to be more closely related to taxa with divergent habitat types, altitudinal distributions and dispersal abilities than they are to populations of restricted endemics that occur in neighbouring montane forest fragments. This repeated transition between lowland and highland habitats over time demonstrate that diversification of the focal group is explained by niche divergence. Our results also highlight an underestimation of diversity compared to morphological studies that has implications for their taxonomy and conservation. Molecular dating suggests that the spatially extensive African radiation arose exceptionally rapidly (1–2.5 Ma) during the fluctuating Plio‐Pleistocene climate, which may have provided the primary driver for lineage diversification.     

When Thailand was an island – the phylogeny and biogeography of mite harvestmen (Opiliones,Cyphophthalmi, Stylocellidae) in Southeast Asia

Aim To develop a comprehensive explanation for the biological diversity of Southeast Asia, especially in the Wallacea and Sundaland regions. This study focuses on a group of arachnids, mite harvestmen, which are thought to be an extremely old group of endemic animals that have been present in the region since most of its land supposedly formed part of the northern rim of the supercontinent Gondwana. Location Eastern Himalayas, Thai‐Malay Peninsula, Sumatra, Borneo, Java, Sulawesi, and New Guinea. Methods  Approximately 5.6 kb of sequence data were obtained from 110 South‐east Asian Cyphophthalmi specimens. Phylogenetic analyses were conducted under a variety of methods and analytical parameters, and the optimal tree was dated using calibration points derived from fossil data. Event based and paralogy‐free subtree biogeographical analyses were conducted. Results The Southeast Asian family Stylocellidae was recovered as monophyletic, arising on what is now the Thai‐Malay Peninsula and diversifying into three main clades. One clade (Meghalaya, here formally placed in Stylocellidae) expanded north as far as the eastern Himalayas, a second clade entered Borneo and later expanded back across the Sundaland Peninsula to Sumatra, and a third clade expanded out of Borneo into the entire lower part of Sundaland. Molecular dating suggested that Stylocellidae separated from other Cyphophthalmi 295 Ma and began diversifying 258 Ma, and the lineage that inhabits mostly Borneo today began diversifying between 175 and 150 Ma. Main conclusions The topology and molecular dating of our phylogenetic hypothesis suggest that Stylocellidae originated on Gondwana, arrived in Southeast Asia via the Cimmerian palaeocontinent, and subsequently diversified north, then south. Their present distribution in the Indo‐Malay Archipelago is explained largely by a diversification over the Sundaland Peninsula before western Sulawesi departed and the peninsula was extensively inundated.     

Deep intra‐island divergence of a montane forest endemic: phylogeography of the Puerto Rican frog Eleutherodactylus portoricensis (Anura: Eleutherodactylidae)

Aim Hypotheses proposed for lineage diversification of tropical montane species have rarely been tested within oceanic islands. Our goal was to understand how basin barriers and Pleistocene climatic fluctuations shaped the distribution of diversity in Eleutherodactylus portoricensis (Eleutherodactylidae), a frog endemic to the montane rain forests of Puerto Rico. Location The north‐eastern (Luquillo) and south‐eastern (Cayey) mountains of Puerto Rico. Methods We generated mitochondrial DNA (mtDNA) control region sequences (c. 565 bp) from 144 individuals of E. portoricensis representing 16 localities, and sequenced 646 bp of cytochrome b and 596 bp of nuclear DNA (nDNA) rhodopsin exon and intron 1 from a subset of individuals. We conducted a phylogenetic analysis on the mtDNA sequence data and explored population substructure with maximum parsimony networks, a spatial analysis of molecular variance, and pairwise F_ST analysis. Coalescent simulations were performed to test alternative models of population divergence in response to late Pleistocene interglacial periods. Historical demography was assessed through coalescent analyses and Bayesian skyline plots. Results We found: (1) two highly divergent groups associated with the disjunct Luquillo and Cayey Mountains, respectively; (2) a shallow mtDNA genetic discontinuity across the La Plata Basin within the Cayey Mountains; (3) phylogeographic congruence between nDNA and mtDNA markers; (4) divergence dates for both mtDNA and nDNA pre‐dating the Holocene interglacial (c. 10 ka), and nDNA suggesting divergence in the penultimate interglacial (c. 245 ka); and (5) historical demographic stability in both lineages. Main conclusions The low‐elevation Caguas Basin is a long‐term barrier to gene flow between the two montane frog populations. Measures of genetic diversity for mtDNA were similar in both lineages, but lower nDNA diversity in the Luquillo Mountains lineage suggests infrequent dispersal between the two mountain ranges and colonization by a low‐diversity founder population. Population divergence began prior to the Holocene interglacial. Stable population sizes over time indicate a lack of demonstrable demographic response to climatic changes during the last glacial period. This study highlights the importance of topographic complexity in promoting within‐island vicariant speciation in the Greater Antilles, and indicates long‐term persistence and lineage diversification despite late Pleistocene climatic oscillations.     

A pre‐Miocene Irano‐Turanian cradle: Origin and diversification of the species‐rich monocot genus Gagea (Liliaceae)

The Irano‐Turanian (IT) floristic region is considered an important center of origin for many taxa. However, there is a lack of studies dealing with typical IT genera that also occur in neighboring areas. The species‐rich monocot genus Gagea Salisb. shows a center of diversity in IT region and a distribution in adjacent regions, therefore representing a good study object to investigate spatial and temporal relationships among IT region and its neighboring areas (East Asia, Euro‐Siberia, Himalaya, and Mediterranean). We aimed at (a) testing the origin of the genus and of its major lineages in the IT region, (b) reconstructing divergence times, and (c) reconstructing colonization events. To address these problems, sequences of the ribosomal DNA internal transcribed spacer (ITS) region of 418 individuals and chloroplast intergenic spacers sequences (psbA‐trnH, trnL‐trnF) of 497 individuals, representing 116 species from all sections of the genus and nearly its entire distribution area were analyzed. Divergence times were estimated under a random molecular clock based on nrITS phylogeny, which was the most complete data set regarding the representation of species and distribution areas. Ancestral distribution ranges were estimated for the nrITS data set as well as for a combined data set, revealing that Gagea most likely originated in southwestern Asia. This genus first diversified there starting in the Early Miocene. In the Middle Miocene, Gagea migrated to the Mediterranean and to East Asia, while migration into Euro‐Siberia took place in the Late Miocene. During the Pleistocene, the Arctic was colonized and Gagea serotina, the most widespread species, reached North America. The Mediterranean basin was colonized multiple times from southwestern Asia or Euro‐Siberia. Most of the currently existing species originated during the last 3 Ma.     

Genetic structure of Micromeria (Lamiaceae) in Tenerife,the imprint of geological history and hybridization on within‐island diversification

Geological history of oceanic islands can have a profound effect on the evolutionary history of insular flora, especially in complex islands such as Tenerife in the Canary Islands. Tenerife results from the secondary connection of three paleo‐islands by a central volcano, and other geological events that further shaped it. This geological history has been shown to influence the phylogenetic history of several taxa, including genus Micromeria (Lamiaceae). Screening 15 microsatellite markers in 289 individuals representing the eight species of Micromeria present in Tenerife, this study aims to assess the genetic diversity and structure of these species and its relation with the geological events on the island. In addition, we evaluate the extent of hybridization among species and discuss its influence on the speciation process. We found that the species restricted to the paleo‐islands present lower levels of genetic diversity but the highest levels of genetic differentiation suggesting that their ranges might have contracted over time. The two most widespread species in the island, M. hyssopifolia and M. varia, present the highest genetic diversity levels and a genetic structure that seems correlated with the geological composition of the island. Samples from M. hyssopifolia from the oldest paleo‐island, Adeje, appear as distinct while samples from M. varia segregate into two main clusters corresponding to the paleo‐islands of Anaga and Teno. Evidence of hybridization and intraspecific migration between species was found. We argue that species boundaries would be retained despite hybridization in response to the habitat's specific conditions causing postzygotic isolation and preserving morphological differentiation.     

Positive selection drives adaptive diversification of the 4‐coumarate: CoA ligase (4CL) gene in angiosperms

Lignin and flavonoids play a vital role in the adaption of plants to a terrestrial environment. 4‐Coumarate: coenzyme A ligase (4CL) is a key enzyme of general phenylpropanoid metabolism which provides the precursors for both lignin and flavonoids biosynthesis. However, very little is known about how such essential enzymatic functions evolve and diversify. Here, we analyze 4CL sequence variation patterns in a phylogenetic framework to further identify the evolutionary forces that lead to functional divergence. The results reveal that lignin‐biosynthetic 4CLs are under positive selection. The majority of the positively selected sites are located in the substrate‐binding pocket and the catalytic center, indicating that nonsynonymous substitutions might contribute to the functional evolution of 4CLs for lignin biosynthesis. The evolution of 4CLs involved in flavonoid biosynthesis is constrained by purifying selection and maintains the ancestral role of the protein in response to biotic and abiotic factors. Overall, our results demonstrate that protein sequence evolution via positive selection is an important evolutionary force driving adaptive diversification in 4CL proteins in angiosperms. This diversification is associated with adaption to a terrestrial environment.     

Linking micro‐ and macroevolutionary perspectives to evaluate the role of Quaternary sea‐level oscillations in island diversification

With shifts in island area, isolation, and cycles of island fusion–fission, the role of Quaternary sea‐level oscillations as drivers of diversification is complex and not well understood. Here, we conduct parallel comparisons of population and species divergence between two island areas of equivalent size that have been affected differently by sea‐level oscillations, with the aim to understand the micro‐ and macroevolutionary dynamics associated with sea‐level change. Using genome‐wide datasets for a clade of seven Amphiacusta ground cricket species endemic to the Puerto Rico Bank (PRB), we found consistently deeper interspecific divergences and higher population differentiation across the unfragmented Western PRB, in comparison to the currently fragmented Eastern PRB that has experienced extreme changes in island area and connectivity during the Quaternary. We evaluate alternative hypotheses related to the microevolutionary processes (population splitting, extinction, and merging) that regulate the frequency of completed speciation across the PRB. Our results suggest that under certain combinations of archipelago characteristics and taxon traits, the repeated changes in island area and connectivity may create an opposite effect to the hypothesized “species pump” action of oscillating sea levels. Our study highlights how a microevolutionary perspective can complement current macroecological work on the Quaternary dynamics of island biodiversity.     

Genomic tests of the species‐pump hypothesis: Recent island connectivity cycles drive population divergence but not speciation in Caribbean crickets across the Virgin Islands

Harnessing the power of genomic scans, we test the debated “species pump” hypothesis that implicates repeated cycles of island connectivity and isolation as drivers of divergence. This question has gone understudied given the limited resolution of past molecular markers for studying such dynamic phenomena. With an average of 32,000 SNPs from the genome of 136 individuals from 10 populations of a Caribbean flightless ground cricket species (Amphiacusta sanctaecrucis) and a complementary set of statistical approaches, we infer a stepping‐stone colonization model and high levels of genetic differentiation across the Virgin Islands, which have been periodically interconnected until 8 ka. Estimates of divergence times from models based on the site frequency spectrum coincide with a period of repeated connection and fragmentation of the islands at 75–130 ka. These results are consistent with a role of island connectivity cycles in promoting genomic divergence and indicate that the genetic distinctiveness of island populations has persisted despite subsequent and extended interisland connections identified from bathymetric data. We discuss these findings in the broader context of Caribbean biogeography, and more specifically why high levels of genomic divergence across the Virgin Islands associated with repeated connectivity cycles do not actually translate into species diversification.     

Miocene diversification of an open‐habitat predatorial passerine radiation,the shrikes (Aves: Passeriformes: Laniidae)

Diversification of avifaunas associated with savannah and steppes appears to correlate with open habitats becoming available, starting in the Miocene. Few comparative analyses exist for families for which all species are predominantly adapted to these habitats. One such group is Laniidae (Passeriformes), which are small‐ to medium‐sized predatory passerines known for their distinctive behaviour of impaling prey. We used multispecies coalescent‐based and concatenation methods to provide the first complete species‐level phylogeny for this group, as well as an estimate of the timing of diversification. Our analyses indicate that Laniidae as currently delimited is not monophyletic, as the genus Eurocephalus is not closely related to the remaining species. The two species currently assigned to the monotypic genera Urolestes and Corvinella are part of the same clade as the Lanius species, and we propose that they are included in the genus Lanius, making Laniidae monogeneric. The initial diversification of the clade is inferred to have occurred very rapidly, starting about 7.2–9.1 million years ago, timing depending on calibration method, but in either case coinciding with the expansion of C4 grasses. An African origin is inferred in the biogeographic analysis. In the redefined Laniidae, cooperative breeding is inferred to be restricted to a single clade, characterized by gregarious behaviour and rallying. Migratory behaviour evolved multiple times within the family.