Why Do Some Lineages Radiate While Others Do Not? Perspectives for Future Research on Adaptive Radiations.

Understanding the processes that drive phenotypic diversification and underpin speciation is key to elucidating how biodiversity has evolved. Although these processes have been studied across a wide array of clades, adaptive radiations (ARs), which are systems with multiple closely related species and broad phenotypic diversity, have been particularly fruitful for teasing apart the factors that drive and constrain diversification. As such, ARs have become popular candidate study systems for determining the extent to which ecological features, including aspects of organisms and the environment, and inter- and intraspecific interactions, led to evolutionary diversification. Despite substantial past empirical and theoretical work, understanding mechanistically how ARs evolve remains a major challenge. Here, we highlight a number of understudied components of the environment and of lineages themselves, which may help further our understanding of speciation and AR. We also outline some substantial remaining challenges to achieving a detailed understanding of adaptation, speciation, and the role of ecology in these processes. These major challenges include identifying factors that have a causative impact in promoting or constraining ARs, gaining a more holistic understanding of features of organisms and their environment that interact resulting in adaptation and speciation, and understanding whether the role of these organismal and environmental features varies throughout the radiation process. We conclude by providing perspectives on how future investigations into the AR process can overcome these challenges, allowing us to glean mechanistic insights into adaptation and speciation.

Neotropics as a Cradle for Adaptive Radiations.

Neotropical ecosystems are renowned for numerous examples of adaptive radiation in both plants and animals resulting in high levels of biodiversity and endemism. However, we still lack a comprehensive review of the abiotic and biotic factors that contribute to these adaptive radiations. To fill this gap, we delve into the geological history of the region, including the role of tectonic events such as the Andean uplift, the formation of the Isthmus of Panama, and the emergence of the Guiana and Brazilian Shields. We also explore the role of ecological opportunities created by the emergence of new habitats, as well as the role of key innovations, such as novel feeding strategies or reproductive mechanisms. We discuss different examples of adaptive radiation, including classic ones like Darwin's finches and Anolis lizards, and more recent ones like bromeliads and lupines. Finally, we propose new examples of adaptive radiations mediated by ecological interactions in their geological context. By doing so, we provide insights into the complex interplay of factors that contributed to the remarkable diversity of life in the Neotropics and highlight the importance of this region in understanding the origins of biodiversity.

Multiple paths toward repeated phenotypic evolution in the spiny-leg adaptive radiation (Tetragnatha; Hawai'i).

The repeated evolution of phenotypes provides clear evidence for the role of natural selection in driving evolutionary change. However, the evolutionary origin of repeated phenotypes can be difficult to disentangle as it can arise from a combination of factors such as gene flow, shared ancestral polymorphisms or mutation. Here, we investigate the presence of these evolutionary processes in the Hawaiian spiny-leg Tetragnatha adaptive radiation, which includes four microhabitat-specialists or ecomorphs, with different body pigmentation and size (Green, Large Brown, Maroon, and Small Brown). We investigated the evolutionary history of this radiation using 76 newly generated low-coverage, whole-genome resequenced samples, along with phylogenetic and population genomic tools. Considering the Green ecomorph as the ancestral state, our results suggest that the Green ecomorph likely re-evolved once, the Large Brown and Maroon ecomorphs evolved twice and the Small Brown evolved three times. We found that the evolution of the Maroon and Small Brown ecomorphs likely involved ancestral hybridization events, while the Green and Large Brown ecomorphs likely evolved through novel mutations, despite a high rate of incomplete lineage sorting in the dataset. Our findings demonstrate that the repeated evolution of ecomorphs in the Hawaiian spiny-leg Tetragnatha is influenced by multiple evolutionary processes.

Evolutionary genomics of oceanic island radiations.

A recurring feature of oceanic archipelagos is the presence of adaptive radiations that generate endemic, species-rich clades that can offer outstanding insight into the links between ecology and evolution. Recent developments in evolutionary genomics have contributed towards solving long-standing questions at this interface. Using a comprehensive literature search, we identify studies spanning 19 oceanic archipelagos and 110 putative adaptive radiations, but find that most of these radiations have not yet been investigated from an evolutionary genomics perspective. Our review reveals different gaps in knowledge related to the lack of implementation of genomic approaches, as well as undersampled taxonomic and geographic areas. Filling those gaps with the required data will help to deepen our understanding of adaptation, speciation, and other evolutionary processes.

Evolutionary drivers of the hump-shaped latitudinal gradient of benthic polychaete species richness along the Southeastern Pacific coast.

Latitudinal diversity gradients (LDG) and their explanatory factors are among the most challenging topics in macroecology and biogeography. Despite of its apparent generality, a growing body of evidence shows that 'anomalous' LDG (i.e., inverse or hump-shaped trends) are common among marine organisms along the Southeastern Pacific (SEP) coast. Here, we evaluate the shape of the LDG of marine benthic polychaetes and its underlying causes using a dataset of 643 species inhabiting the continental shelf (<200 m depth), using latitudinal bands with a spatial resolution of 0.5°, along the SEP (3-56° S). The explanatory value of six oceanographic (Sea Surface Temperature (SST), SST range, salinity, salinity range, primary productivity and shelf area), and one macroecological proxy (median latitudinal range of species) were assessed using a random forest model. The taxonomic structure was used to estimate the degree of niche conservatism of predictor variables and to estimate latitudinal trends in phylogenetic diversity, based on three indices (phylogenetic richness (PDSES), mean pairwise distance (MPDSES), and variation of pairwise distances (VPD)). The LDG exhibits a hump-shaped trend, with a maximum peak of species richness at ca. 42° S, declining towards northern and southern areas of SEP. The latitudinal pattern was also evident in local samples controlled by sampling effort. The random forest model had a high accuracy (pseudo-r2 = 0.95) and showed that the LDG could be explained by four variables (median latitudinal range, SST, salinity, and SST range), yet the functional relationship between species richness and these predictors was variable. A significant degree of phylogenetic conservatism was detected for the median latitudinal range and SST. PDSES increased toward the southern region, whereas VPD showed the opposite trend, both statistically significant. MPDSES has the same trend as PDSES, but it is not significant. Our results reinforce the idea that the south Chile fjord area, particularly the Chiloé region, was likely the evolutionary source of new species of marine polychaetes along SEP, creating a hotspot of diversity. Therefore, in the same way as the canonical LDG shows a decline in diversity while moving away from the tropics; on this case the decline occurs while moving away from Chiloé Island. These results, coupled with a strong phylogenetic signal of the main predictor variables suggest that processes operating mainly at evolutionary timescales govern the LDG.

Beetle Diversity Across Micro-habitats on Lizard Island Group (Great Barrier Reef, Australia).

The beetles (Coleoptera) of Lizard Island group, a complex of small granitic islands on the Great Barrier Reef, have never been systematically assessed. In April 2019, we conducted the first survey of the island group across different micro-habitats. We specifically aimed to determine which beetle families are the most diverse, and how beetle diversity varies across the island group. We sampled several sites on seven large collection areas using a variety of methods: pitfall traps, beating sheet, sifting leaf litter, and active night and day collection. Our sampling yielded 108 beetle morphospecies representing at least 21 families. The most diverse families on Lizard Island group were Curculionidae, Carabidae, Scarabaeidae, Tenebrionidae, and Cerambycidae, in general accordance with global patterns in Coleoptera diversity. The families Chrysomelidae, Staphylinidae, and Buprestidae were found to be proportionally less diverse on the island group than on mainland Australia, though Australia as a whole is of limited value as a reference. Beetle diversity varied across both large-scale collection areas and small-scale collection sites on Lizard Island group. As expected, greater habitat complexity and vegetation diversity corresponded with greater beetle diversity, though these patterns might be biased due to the temporal and spatial limits of our sampling. We hope this preliminary survey will facilitate further research on Lizard Island group, taking advantage of the research facilities on the island and the possibility of establishing long-term studies.

Implications of a cheliceral axial duplication in Tetragnatha versicolor (Araneae: Tetragnathidae) for arachnid deuterocerebral appendage development.

The homology of the arachnid chelicera with respect to other head appendages in Panarthropoda has long been debated. Gene expression data and the re-interpretation of early transitional fossils have supported the homology of the deutocerebrum and its associated appendages, implying a homology between primary antennae (mandibulates), chelicerae (euchelicerates), and chelifores (sea spiders). Nevertheless, comparatively little is known about the mechanistic basis of proximo-distal (PD) axis induction in chelicerates, much less the basis for cheliceral fate specification. Here, we describe a new cheliceral teratology in the spider Tetragnatha versicolor Walckenaer, 1841, which consists on a duplication of the PD axis of the left chelicera associated with a terminal secondary schistomely on the fang of the lower axis. This duplication offers clues as to potential shared mechanisms of PD axis formation in the chelicera. We review the state of knowledge on PD axis induction mechanisms in arthropods and identify elements of gene regulatory networks that are key for future functional experiments of appendage development in non-insect model systems. Such investigations would allow a better understanding of PD axis induction of modified and poorly studied arthropod limbs (e.g., chelicerae, chelifores, and ovigers).

Intraspecific niche partition without speciation: individual level web polymorphism within a single island spider population.

Early in the process of adaptive radiation, allopatric disruption of gene flow followed by ecological specialization is key for speciation; but, do adaptive radiations occur on small islands without internal geographical barriers? Island populations sometimes harbour polymorphism in ecological specializations, but its significance remains unclear. On one hand, morphs may correspond to 'cryptic' species. Alternatively, they could result from population, developmental or behavioural plasticity. The spider Wendilgarda galapagensis (Araneae, Theridiosomatidae) is endemic to the small Isla del Coco and unique in spinning three different web types, each corresponding to a different microhabitat. We tested whether this variation is associated with 'cryptic' species or intraspecific behavioural plasticity. Despite analysing 36 803 loci across 142 individuals, we found no relationship between web type and population structure, which was only weakly geographically differentiated. The same pattern holds when looking within a sampling site or considering only Fst outliers. In line with genetic data, translocation experiments showed that web architecture is plastic within an individual. However, not all transitions between web types are equally probable, indicating the existence of individual preferences. Our data supports the idea that diversification on small islands might occur mainly at the behavioural level producing an intraspecific niche partition without speciation.

Annotated list of island lady beetles from Chile (Coleoptera: Coccinellidae).

We provide a list of coccinellids (Coleoptera: Coccinellidae) species from the island territories of Chile. We report a total of 68 records, coming from ten islands, including 42 species corresponding to more than 35% of the species of the country. This paper presents the first Coccinellidae records for the Islas Desventuradas, Isla Mocha and Isla Tenglo. Contrary to what has been reported on other islands and other taxonomic groups in Chilean islands, the level of coccinellid endemism is low (8%), with only one and two species endemic to the Juan Fernández archipelago and Isla de Chiloé, respectively, and probably a fourth species from the Isla Grande de Tierra del Fuego. The presence of species with worldwide distribution and of agricultural relevance is strong in the Chilean oceanic islands, particularly in Rapa Nui. The fauna of the continental islands is very similar to the one in the nearby continental areas and composed of native species. Further surveys of Coccinellidae and other insects are required for the islands of Chile, especially for several of them in which there are no records.

Aerial plankton from the Eastern Tropical Pacific

Introduction: Small terrestrial invertebrates disperse in a passive manner through wind currents, forming what is known as aerial plankton, which has not been surveyed yet for the Eastern Tropical Pacific. Documenting the aerial plankton of Isla del Coco will allow to better understand the colonization process of this highly diverse island. Objective: Characterize the aerial plankton present on the transect Puntarenas - Isla del Coco. Methods: Specimens were collected using entomological nets on 2 roundtrip voyages during the months of July and August of 2017 and 2018, respectively. Results: A total of 10 morpho-species were collected corresponding to the orders: Diptera (Ceratopogonidae, Milichiidae, and Nematocera of a non-identified family), Hymenoptera (Chalcidoidea: Agaonidae), Hemiptera (Scutelleridae and Coreidae) and Lepidoptera (Sphingidae). Diptera and Hymenoptera were collected on the nets; while, Hemiptera and Lepidoptera were found on the deck of the boat. No spiders were collected. The Diptera and Hymenoptera families, as well as the family Coreidae (Hemiptera), have been previously recorded on this type of surveys across the tropical Pacific. Conclusions: Two of the taxa collected by nets, Ceratopogonidae (Diptera) and Chalcidoidea (Hymenoptera), have representatives on Isla del Coco, which could provide direct support for wind dispersal as a colonization mechanism for these groups. We also detected other insects (i.e. Lepidoptera and Scutelleridae-Hemiptera) which most likely reached the boat by their own means providing evidence of their dispersal abilities. This research provides data to further expand on questions about the mechanisms of island colonization.

Introducción: Los invertebrados terrestres pequeños se dispersan de manera pasiva en corrientes de viento, constituyendo lo que se conoce como plancton aéreo, el cual previamente no había sido evaluado en Pacífico Tropical Oriental (PTO). Documentar el plancton aéreo de la Isla del Coco permitiría entender mejor el proceso de colonización de esta diversa isla. Objetivos: Caracterizar el plancton aéreo del transecto Puntarenas - Isla del Coco. Métodos: Los especímenes fueron recolectados utilizando redes entomológicas en 2 viajes de ida y vuelta durante los meses de Julio y Agosto de 2017 y 2018, respectivamente. Resultados: Un total de 10 morfo-especies fueron recolectadas, correspondientes a los órdenes Diptera (Ceratopogonidae, Milichiidae, y Nematocera de familia no identificada), Hymenoptera (Chalcidoidea: Agaonidae), Hemiptera (Scutelleridae y Coreidae) y Lepidoptera (Sphingidae). Diptera e Hymenoptera fueron recolectados en las redes; mientras que Hemiptera y Lepidoptera fueron encontrados en la cubierta del barco. No se recolectaron arañas. Las familias de Diptera e Hymenoptera, al igual que la familia Coreidae (Hemiptera) han sido previamente registradas en este tipo de muestreos en el PTO. Conclusiones: Dos de los taxones recolectados en las redes, Ceratopogonidae (Diptera) y Chalcidoidea (Hymenoptera), están representados en la Isla del Coco, lo cual provee apoyo directo a la dispersión por viento como un mecanismo de colonización para estos grupos. Igualmente, encontramos otros insectos (Lepidoptera y Hemiptera: Scutelleridae), los cuales probablemente llegaron al barco por sus propios medios, evidenciando sus habilidades de dispersión. Esta investigación entrega datos para responder nuevas preguntas sobre los mecanismos de colonización de islas.

First endemic arachnid from Isla Sala y Gómez (Motu Motiro Hiva), Chile: a new species of tube-dwelling spider (Araneae: Segestriidae)

The Isla Sala y Gómez or Motu Motiro Hiva is located 415 km northeast of Rapa Nui (Easter Island) and 3420 km from the coast of northern Chile. It is a small oceanic island (2.5 km2) dominated by volcanic rock with very little vegetal cover. Here, we describe the first endemic arachnid for the island, Ariadna motumotirohiva sp. nov. Females are similar to those of Ariadna perkinsi Simon, 1900 from Hawaiʻi and Ariadna lebronneci Berland, 1933 from the Marquesas in the dorsal dark abdominal pattern, but they differentiate from the latter in the anterior receptaculum, promarginal cheliceral teeth and leg IV macrosetae. A recent survey of the arachnid fauna of Rapa Nui, which included Motu Nui and the rocky shores, did not record the presence of the family Segestriidae, neither has it been found during previous surveys. However, it is not possible to discard the possibility of a local extinction on Rapa Nui and survival on Sala y Gómez. This study suggests other endemic terrestrial arthropods could be present on this very small and remote island.

Co-occurrence of ecologically similar species of Hawaiian spiders reveals critical early phase of adaptive radiation.

BACKGROUND: The processes through which populations originate and diversify ecologically in the initial stages of adaptive radiation are little understood because we lack information on critical steps of early divergence. A key question is, at what point do closely related species interact, setting the stage for competition and ecological specialization? The Hawaiian Islands provide an ideal system to explore the early stages of adaptive radiation because the islands span ages from 0.5-5 Mya. Hawaiian spiders in the genus Tetragnatha have undergone adaptive radiation, with one lineage ("spiny legs") showing four different ecomorphs (green, maroon, large brown, small brown); one representative of each ecomorph is generally found at any site on the older islands. Given that the early stages of adaptive radiation are characterized by allopatric divergence between populations of the same ecomorph, the question is, what are the steps towards subsequent co-occurrence of different ecomorphs? Using a transcriptome-based exon capture approach, we focus on early divergence among close relatives of the green ecomorph to understand processes associated with co-occurrence within the same ecomorph at the early stages of adaptive radiation. RESULTS: The major outcomes from the current study are first that closely related species within the same green ecomorph of spiny leg Tetragnatha co-occur on the same single volcano on East Maui, and second that there is no evidence of genetic admixture between these ecologically equivalent species. Further, that multiple genetic lineages exist on a single volcano on Maui suggests that there are no inherent dispersal barriers and that the observed limited distribution of taxa reflects competitive exclusion. CONCLUSIONS: The observation of co-occurrence of ecologically equivalent species on the young volcano of Maui provides a missing link in the process of adaptive radiation between the point when recently divergent species of the same ecomorph occur in allopatry, to the point where different ecomorphs co-occur at a site, as found throughout the older islands. More importantly, the ability of close relatives of the same ecomorph to interact, without admixture, may provide the conditions necessary for ecological divergence and independent evolution of ecomorphs associated with adaptive radiation.

Squeezing water from a stone: high-throughput sequencing from a 145-year old holotype resolves (barely) a cryptic species problem in flying lizards.

We used Massively Parallel High-Throughput Sequencing to obtain genetic data from a 145-year old holotype specimen of the flying lizard, Draco cristatellus. Obtaining genetic data from this holotype was necessary to resolve an otherwise intractable taxonomic problem involving the status of this species relative to closely related sympatric Draco species that cannot otherwise be distinguished from one another on the basis of museum specimens. Initial analyses suggested that the DNA present in the holotype sample was so degraded as to be unusable for sequencing. However, we used a specialized extraction procedure developed for highly degraded ancient DNA samples and MiSeq shotgun sequencing to obtain just enough low-coverage mitochondrial DNA (721 base pairs) to conclusively resolve the species status of the holotype as well as a second known specimen of this species. The holotype was prepared before the advent of formalin-fixation and therefore was most likely originally fixed with ethanol and never exposed to formalin. Whereas conventional wisdom suggests that formalin-fixed samples should be the most challenging for DNA sequencing, we propose that evaporation during long-term alcohol storage and consequent water-exposure may subject older ethanol-fixed museum specimens to hydrolytic damage. If so, this may pose an even greater challenge for sequencing efforts involving historical samples.

Ancient DNA Resolves the History of Tetragnatha (Araneae, Tetragnathidae) Spiders on Rapa Nui.

Rapa Nui is one of the most remote islands in the world. As a young island, its biota is a consequence of both natural dispersals over the last ~1 million years and recent human introductions. It therefore provides an opportunity to study a unique community assemblage. Here, we extract DNA from museum-preserved and newly field-collected spiders from the genus Tetragnatha to explore their history on Rapa Nui. Using an optimized protocol to recover ancient DNA from museum-preserved spiders, we sequence and assemble partial mitochondrial genomes from nine Tetragnatha species, two of which were found on Rapa Nui, and estimate the evolutionary relationships between these and other Tetragnatha species. Our phylogeny shows that the two Rapa Nui species are not closely related. One, the possibly extinct, T. paschae, is nested within a circumtropical species complex (T. nitens), and the other (Tetragnatha sp. Rapa Nui) appears to be a recent human introduction. Our results highlight the power of ancient DNA approaches in identifying cryptic and rare species, which can contribute to our understanding of the global distribution of biodiversity in all taxonomic lineages.