Data from: Divergence of tropical pitvipers promoted by independent colonization events of dry montane Andean habitats
Contributors: Salazar-Valenzuela, David, Kuch, Ulrich, Torres-Carvajal, Omar, Valencia, Jorge H., Gibbs, H. Lisle
... Aim: One aspect that is still poorly explored about the origin and maintenance of Neotropical biodiversity is how the evolutionary dynamics of colonization and differentiation in relation to lowland and highland habitats has impacted lineage formation. Most speciation models for this region have focused on vicariant events, and the need to assess the influence of demographic processes has been recognized only recently. We evaluate if the origin of Andean montane lineages of terciopelo pitvipers is explained by either of two historical processes that represent fundamental phylogeographic mechanisms: differentiation by isolation within the highlands or different dispersal events from the lowlands. Location: Western Ecuador. Taxon: Terciopelo pitvipers (Bothrops asper species complex). Methods: We use genomic data and genetic clustering analyses, evaluation of historical migration between genetic clusters, and demographic model selection to investigate recent diversification events in South America using a vertebrate group rarely explored in phylogeographic studies: tropical Andean snakes. Specifically, the origin of two Ecuadorian montane lineages of terciopelo pitvipers was evaluated given ambiguous phylogenetic relationships with the presumably ancestral Pacific lowland lineage. Results: Discrepancies of evolutionary relationships previously obtained with tree-like methods are resolved through the use of modeling approaches. We found strong support for the independent origin of montane lineages based on topologies inferred by maximum-likelihood trees and modeling approaches that take into account possible gene flow. Main conclusions: Recent large-scale studies have found support for identifying dispersal events as important drivers of diversification in the Neotropical region. We contribute to these ideas by identifying a fine-scale case in a rarely explored group of animals -Andean snakes- in which river valleys acted as an entrance for the upward colonization of montane dry habitats and subsequent ecological diversification.
Contributors: Burford Reiskind, Martha O., Labadie, Paul E, Bargielowski, Irka, Lounibos, L. Philip, Reiskind, Michael H.
... While few species introduced into a new environment become invasive, those that do provide critical information on ecological mechanisms that determine invasions success and the evolutionary responses that follow invasion. Aedes albopictus (the Asian tiger mosquito) was introduced into the naturalized range of Aedes aegypti (the yellow fever mosquito) in the USA in the mid-1980s, resulting in the displacement of A. aegypti in much of the southeastern USA. The rapid displacement was likely due to the superior competitive ability of A. albopictus as larvae and asymmetric mating interference competition, in which male A. albopictus mate with and sterilize A. aegypti females, a process called “satyrization”. The goal of this study was to examine the genomic responses of a resident species to an invasive species in which the mechanism of character displacement is understood. We used double-digest restriction enzyme DNA sequencing (ddRADseq) to analyze outlier loci between selected and control lines of laboratory-reared A. aegypti females from two populations (Tucson, AZ and Key West, Florida, USA), and individual females classified as either “resisted” or “mated with” A. albopictus males via mating trials of wild-derived females from four populations in Florida. We found significant outlier loci in comparing selected and control lines and between mated and non-mated A. aegypti females in the laboratory and wild-derived populations, respectively. We found overlap in specific outlier loci between different source populations that support consistent genomic signatures of selection within A. aegypti. Our results point to regions of the A. aegypti genome and potential candidate genes that may be involved in mating behavior, and specifically in avoiding interspecific mating choices.
Data from: Using the Mus musculus hybrid zone to assess covariation and genetic architecture of limb bone lengths
Contributors: Skrabar, Neva, Turner, Leslie M., Pallares, Luisa F., Harr, Bettina, Tautz, Diethard
... Two subspecies of the house mouse, Mus musculus domesticus and Mus musculus musculus, meet in a narrow contact zone across Europe. Mice in the hybrid zone are highly admixed, representing the full range of mixed ancestry from the two subspecies. Given the distinct morphologies of these subspecies, these natural hybrids can be used for genome-wide association mapping at sufficiently high resolution to directly infer candidate genes. We focus here on limb bone length differences, which is of special interest for understanding the evolution of developmentally correlated traits. We used 172 first-generation descendants of wild-caught mice from the hybrid zone to measure the length of stylopod (humerus / femur), zeugopod (ulna / tibia) and autopod (metacarpal / metatarsal) elements in skeletal CT scans. We find phenotypic covariation between limb elements in the hybrids similar to patterns previously described in M. m. domesticus inbred strains, suggesting that the hybrid genotypes do not influence the covariation pattern in a major way. Mapping was performed using 143,592 SNPs and identified several genomic regions associated with length differences in each bone. Each candidate region explains only a small proportion of phenotypic variance, suggesting that bone length is highly polygenic. None of the candidate regions includes the canonical genes known to control embryonic limb development. Instead, we are able to identify candidate genes with known roles in osteoblast differentiation and bone structure determination, as well as recently evolved genes of, as yet, unknown function.
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Data from: How sea-level change mediates genetic divergence in coastal species across regions with varying tectonic and sediment processes
Contributors: Dolby, Greer A., Ellingson, Ryan A., Findley, Lloyd T., Jacobs, David K.
... Plate tectonics and sediment processes control regional continental shelf topography. We examine the genetic consequences of how glacial-associated sea-level change interacted with variable near-shore topography since the last glaciation. We reconstructed the size and distribution of areas suitable for tidal estuary formation from the Last Glacial Maximum, ~20 thousand years ago, to present from San Francisco, California, USA (~38 °N) to Reforma, Sinaloa, Mexico (~25 °N). We assessed range-wide genetic structure and diversity of three co-distributed tidal estuarine fishes (California Killifish, Shadow Goby, Longjaw Mudsucker) along ~4,600 km using mitochondrial control region and cytB sequence, and 16–20 microsatellite loci from a total of 524 individuals. Results show that glacial-associated sea-level change limited estuarine habitat to few, widely separated refugia at glacial lowstand, and present-day genetic clades were sourced from specific refugia. Habitat increased during postglacial sea-level rise and refugial populations admixed in newly formed habitats. Continental shelves with active tectonics and/or low sediment supply were steep and hosted fewer, smaller refugia with more genetically differentiated populations than on broader shelves. Approximate Bayesian computation favored the refuge-recolonization scenarios from habitat models over isolation by distance and seaway alternatives, indicating isolation at lowstand is a major diversification mechanism among estuarine (and perhaps other) coastal species. Because sea-level change is a global phenomenon, we suggest this top-down physical control of extirpation-isolation-recolonization may be an important driver of genetic diversification in coastal taxa inhabiting other topographically complex coasts globally during the Mid- to Late Pleistocene and deeper timescales.
Data from: Habitat continuity and stepping-stone oceanographic distances explain population genetic connectivity of the brown alga Cystoseira amentacea
Contributors: Buonomo, Roberto, Assis, Jorge, Fernandes, Francisco, Engelen, Aschwin H., Airoldi, Laura, Serrão, Ester A.
... Effective predictive and management approaches for species occurring in a metapopulation structure require good understanding of inter-population connectivity. In this study we ask whether population genetic structure of marine species with fragmented distributions can be predicted by stepping-stone oceanographic transport and habitat continuity, using as model an ecosystem-structuring brown alga, Cystoseira amentacea var. stricta. To answer this question, we analyzed the genetic structure and estimated the connectivity of populations along discontinuous rocky habitat patches in southern Italy, using microsatellite markers at multiple scales. In addition, we modelled the effect of rocky habitat continuity and ocean circulation on gene flow by simulating Lagrangian particle dispersal based on ocean surface currents allowing multigenerational stepping-stone dynamics. Populations were highly differentiated, at scales from few meters up to 1000s of kilometers. The best possible model fit to explain the genetic results combined current direction, rocky habitat extension and distance along the coast among rocky sites. We conclude that a combination of variables suitable habitat and oceanographic transport is a useful predictor of genetic structure. This relationship provides insight into the mechanisms of dispersal and the role of life history traits. Our results highlight the importance of spatially explicit modeling of stepping stone dynamics and oceanographic directional transport coupled with habitat suitability, to better describe and predict marine population structure and differentiation. This study also suggests the appropriate spatial scales for the conservation, restoration and management of species that are increasingly affected by habitat modifications.
Contributors: Alexandri, Panoraia, Megens, Hendrik-Jan, Crooijmans, Richard P. M. A., Groenen, Martien A. M., Goedbloed, Daniel J., Herrero-Medrano, Juan M., Rund, Lauretta A., Schook, Lawrence B., Chatzinikos, Evangelos, Triantaphyllidis, Costas
... Aim: We compared the power of different nuclear markers to investigate genetic structure of southern Balkan wild boar. We distinguished between historic events, such as isolation in different refugia during glacial periods, from recent demographic processes, such as naturally occurring expansions. Location: Southern Balkans/Greece. Methods: We sampled 555 wild boars from 20 different locations in southern Balkans/Greece. All individuals were analysed with 10 microsatellites and a subgroup of 91 with 49,508 single nucleotide polymorphisms (SNPs). Patterns of genetic structure and demographic processes were assessed with Bayesian clustering, linkage disequilibrium and past effective population size estimation analysis. Results: Both microsatellite and SNP data analyses detected genetic structure caused by historic events and support the existence of three groups in the studied area. A hybrid zone between two of the groups was also detected. We also showed that genome-wide SNP data analysis can identify recent events in bottlenecked populations. Main conclusions: We inferred the three groups diverged ~50,000–10,000 yr bp when populations contracted to different refugia. Our findings strengthened the evidence that the southern Balkan area was a glacial refugium including further local smaller refugia. Genome-wide genotyping inferred a recent population expansion that can mimic a ‘refugium within refugium’ scenario. It seems that microsatellite data tend to overestimate genetic structure when genetic drift happens in bottlenecked populations over a short distance. Therefore, genome-wide SNPs are more powerful at inferring phylogeography in natural populations, resolving inconsistencies from mitochondrial and microsatellite data sets.
Data from: Comparative cranial myology and biomechanics of Plateosaurus and Camarasaurus and evolution of the sauropod feeding apparatus
Contributors: Button, David J., Barrett, Paul M., Rayfield, Emily J.
... Sauropodomorpha represents an important group of Mesozoic megaherbivores, and includes the largest terrestrial animals ever known. It was the first dinosaur group to become abundant and widespread, and its members formed a significant component of terrestrial ecosystems from the Late Triassic until the end of the Cretaceous. Both of these factors have been explained by their adoption of herbivory, but understanding the evolution of sauropodomorph feeding has been hampered by the scarcity of biomechanical studies. To address this, the jaw adductor musculature of the basal sauropodomorph Plateosaurus and the sauropod Camarasaurus have been reconstructed. These reconstructions provide boundary conditions for finite element models to assess differences in structural performance between the two taxa. Results demonstrate that Camarasaurus was capable of much greater bite forces than Plateosaurus, due to greater relative adductor muscle mass and shape changes to the mandible. The skull and mandible of Camarasaurus are also ‘stronger’ under static biting. The Plateosaurus mandible appears to compromise structural efficiency and force transmission in order to maintain relatively high jaw closure speed. This supports suggestions of facultative omnivory in basal sauropodomorph taxa. The expanded mandibular symphysis and ‘lateral plates’ of sauropods each lead to greater overall craniomandibular robustness, and may have been especially important in accommodating forces related to asymmetric loading. The functional roles of these characters, and observed general shape changes in increasing skull robustness, are consistent with hypotheses linking bulk-herbivory with the origin of Sauropoda and the evolution of gigantism.
Data from: Demographic modelling with whole-genome data reveals parallel origin of similar Pundamilia cichlid species after hybridization
Contributors: Meier, Joana I., Sousa, Vitor C., Marques, David Alexander, Selz, Oliver M., Wagner, Catherine E., Excoffier, Laurent, Seehausen, Ole
... Modes and mechanisms of speciation are best studied in young species pairs. In older taxa, it is increasingly difficult to distinguish what happened during speciation from what happened after speciation. Lake Victoria cichlids in the genus Pundamilia encompass a complex of young species and polymorphic populations. One Pundamilia species pair, P. pundamilia and P. nyererei, is particularly well suited to study speciation because sympatric population pairs occur with different levels of phenotypic differentiation and reproductive isolation at different rocky islands within the lake. Genetic distances between allopatric island populations of the same nominal species often exceed those between the sympatric species. It thus remained unresolved whether speciation into P. nyererei and P. pundamilia occurred once, followed by geographical range expansion and interspecific gene flow in local sympatry, or if the species pair arose repeatedly by parallel speciation. Here, we use genomic data and demographic modelling to test these alternative evolutionary scenarios. We demonstrate that gene flow plays a strong role in shaping the observed patterns of genetic similarity, including both gene flow between sympatric species and gene flow between allopatric populations, as well as recent and early gene flow. The best supported model for the origin of P. pundamilia and P. nyererei population pairs at two different islands is one where speciation happened twice, whereby the second speciation event follows shortly after introgression from an allopatric P. nyererei population that arose earlier. Our findings support the hypothesis that very similar species may arise repeatedly, potentially facilitated by introgressed genetic variation.
Contributors: Richardson, Mark F., Sherman, Craig D. H., Lee, Randall S., Bott, Nathan J., Hirst, Alastair J.
... The establishment and subsequent spread of invasive species is widely recognized as one of the most threatening processes contributing to global biodiversity loss. This is especially true for marine and estuarine ecosystems, which have experienced significant increases in the number of invasive species with the increase in global maritime trade. Understanding the rate and mechanisms of range expansion is therefore of significant interest to ecologists and conservation managers alike. Using a combination of population genetic surveys, environmental DNA (eDNA) plankton sampling and hydrodynamic modelling, we examined the patterns of introduction of the predatory Northern Pacific seastar (Asterias amurensis) and pathways of secondary spread within southeast Australia. Genetic surveys across the invasive range reveal some genetic divergence between the two main invasive regions and no evidence of ongoing gene flow, a pattern that is consistent with the establishment of the second invasive region via a human-mediated translocation event. In contrast, hydrodynamic modelling combined with eDNA plankton sampling demonstrated that the establishment of range expansion populations within a region is consistent with natural larval dispersal and recruitment. Our results suggest that both anthropogenic and natural dispersal vectors have played an important role in the range expansion of this species in Australia. The multiple modes of spread combined with high levels of fecundity and a long larval duration in A. amurensis suggests it is likely to continue its range expansion and significantly impact Australian marine ecosystems.
Data from: Contrasting support for alternative models of genomic variation based on microhabitat preference: species-specific effects of climate change in alpine sedges
Contributors: Massatti, Rob, Knowles, L. Lacey
... Deterministic processes may uniquely affect codistributed species’ phylogeographic patterns such that discordant genetic variation among taxa is predicted. Yet, explicitly testing expectations of genomic discordance in a statistical framework remains challenging. Here, we construct spatially and temporally dynamic models to investigate the hypothesized effect of microhabitat preferences on the permeability of glaciated regions to gene flow in two closely related montane species. Utilizing environmental niche models from the Last Glacial Maximum and the present to inform demographic models of changes in habitat suitability over time, we evaluate the relative probabilities of two alternative models using approximate Bayesian computation (ABC) in which glaciated regions are either (i) permeable or (ii) a barrier to gene flow. Results based on the fit of the empirical data to data sets simulated using a spatially explicit coalescent under alternative models indicate that genomic data are consistent with predictions about the hypothesized role of microhabitat in generating discordant patterns of genetic variation among the taxa. Specifically, a model in which glaciated areas acted as a barrier was much more probable based on patterns of genomic variation in Carex nova, a wet-adapted species. However, in the dry-adapted Carex chalciolepis, the permeable model was more probable, although the difference in the support of the models was small. This work highlights how statistical inferences can be used to distinguish deterministic processes that are expected to result in discordant genomic patterns among species, including species-specific responses to climate change.