Integrating biogeography and behavioral ecology to rapidly address biodiversity loss.

Addressing climate change and biodiversity loss will be the defining ecological, political, and humanitarian challenge of our time. Alarmingly, policymakers face a narrowing window of opportunity to prevent the worst impacts, necessitating complex decisions about which land to set aside for biodiversity preservation. Yet, our ability to make these decisions is hindered by our limited capacity to predict how species will respond to synergistic drivers of extinction risk. We argue that a rapid integration of biogeography and behavioral ecology can meet these challenges because of the distinct, yet complementary levels of biological organization they address, scaling from individuals to populations, and from species and communities to continental biotas. This union of disciplines will advance efforts to predict biodiversity's responses to climate change and habitat loss through a deeper understanding of how biotic interactions and other behaviors modulate extinction risk, and how responses of individuals and populations impact the communities in which they are embedded. Fostering a rapid mobilization of expertise across behavioral ecology and biogeography is a critical step toward slowing biodiversity loss.

Population demography maintains biogeographic boundaries.

Global biodiversity is organised into biogeographic regions that comprise distinct biotas. The contemporary factors maintaining differences in species composition between regions are poorly understood. Given evidence that populations with sufficient genetic variation can adapt to fill new habitats, it is surprising that more homogenisation of species assemblages across regions has not occurred. Theory suggests that expansion across biogeographic regions could be limited by reduced adaptive capacity due to demographic variation along environmental gradients, but this possibility has not been empirically explored. Using three independently curated data sets describing continental patterns of mammalian demography and population genetics, we show that populations near biogeographic boundaries have lower effective population sizes and genetic diversity, and are more genetically differentiated. These patterns are consistent with reduced adaptive capacity in areas where one biogeographic region transitions into the next. That these patterns are replicated across mammals suggests they are stable and generalisable in their contribution to long-term limits on biodiversity homogenisation. Understanding the contemporary processes that maintain compositional differences among regional biotas is crucial for our understanding of the current and future organisation of global biodiversity.

Dispersal barriers and opportunities drive multiple levels of phylogeographic concordance in the Southern Alps of New Zealand.

Phylogeographic concordance, or the sharing of phylogeographic patterns among codistributed species, suggests similar responses to topography or climatic history. While the orientation and timing of breaks between lineages are routinely compared, spatial dynamics within regions occupied by individual lineages provide a second opportunity for comparing responses to past events. In environments with complex topography and glacial history, such as New Zealand's South Island, geographically nested comparisons can identify the processes leading to phylogeographic concordance between and within regional genomic clusters. Here, we used single nucleotide polymorphisms (obtained via ddRADseq) for two codistributed forest beetle species, Agyrtodes labralis (Leiodidae) and Brachynopus scutellaris (Staphylinidae), to evaluate the role of climate change and topography in shaping phylogeographic concordance at two, nested spatial scales: do species diverge over the same geographic barriers, with similar divergence times? And within regions delimited by these breaks, do species share similar spatial dynamics of directional expansion or isolation-by-distance? We found greater congruence of phylogeographic breaks between regions divided by the strongest dispersal barriers (i.e., the Southern Alps). However, these shared breaks were not indicative of shared spatial dynamics within the regions they delimit, and the most similar spatial dynamics between species occurred within regions with the strongest gradients in historical climatic stability. Our results indicate that lack of concordance as traditionally detected by lineage turnover does not rule out the possibility of shared histories, and variation in the presence and type of concordance may provide insights into the different processes shaping phylogeographic patterns across geologically dynamic regions.

Species-specific responses of Late Quaternary megafauna to climate and humans.

Despite decades of research, the roles of climate and humans in driving the dramatic extinctions of large-bodied mammals during the Late Quaternary period remain contentious. Here we use ancient DNA, species distribution models and the human fossil record to elucidate how climate and humans shaped the demographic history of woolly rhinoceros, woolly mammoth, wild horse, reindeer, bison and musk ox. We show that climate has been a major driver of population change over the past 50,000 years. However, each species responds differently to the effects of climatic shifts, habitat redistribution and human encroachment. Although climate change alone can explain the extinction of some species, such as Eurasian musk ox and woolly rhinoceros, a combination of climatic and anthropogenic effects appears to be responsible for the extinction of others, including Eurasian steppe bison and wild horse. We find no genetic signature or any distinctive range dynamics distinguishing extinct from surviving species, emphasizing the challenges associated with predicting future responses of extant mammals to climate and human-mediated habitat change.

Process-Based Species Pools Reveal the Hidden Signature of Biotic Interactions Amid the Influence of Temperature Filtering.

A persistent challenge in ecology is to tease apart the influence of multiple processes acting simultaneously and interacting in complex ways to shape the structure of species assemblages. We implement a heuristic approach that relies on explicitly defining species pools and permits assessment of the relative influence of the main processes thought to shape assemblage structure: environmental filtering, dispersal limitations, and biotic interactions. We illustrate our approach using data on the assemblage composition and geographic distribution of hummingbirds, a comprehensive phylogeny and morphological traits. The implementation of several process-based species pool definitions in null models suggests that temperature-but not precipitation or dispersal limitation-acts as the main regional filter of assemblage structure. Incorporating this environmental filter directly into the definition of assemblage-specific species pools revealed an otherwise hidden pattern of phylogenetic evenness, indicating that biotic interactions might further influence hummingbird assemblage structure. Such hidden patterns of assemblage structure call for a reexamination of a multitude of phylogenetic- and trait-based studies that did not explicitly consider potentially important processes in their definition of the species pool. Our heuristic approach provides a transparent way to explore patterns and refine interpretations of the underlying causes of assemblage structure.

Phylogeography reveals the complex impact of the Last Glacial Maximum on New Zealand's terrestrial biota.

We review the major phylogeographic patterns in Aotearoa New Zealand's terrestrial flora and fauna that have been associated with the Otira Glaciation of the Pleistocene, the end of which coincides with the global Last Glacial Maximum (LGM). We focus on (1) the complexity of biogeographic histories of New Zealand species, with LGM-driven phenomena overlaying the impacts of mountain-building and other drivers of phylogeographic structure; (2) the locations of glacial refugia and sets of taxa which may have shared refugia; and (3) the role of glaciation in driving diversification. We end with a brief focus on the next directions, including what can we learn about New Zealand's glacial history by expanding our phylogeographic toolbox to include genomic methods and hypothesis-driven inference methods. We provide follow-up questions which take advantage of the wealth of phylogeographic data for New Zealand.

Global determinants of insect mitochondrial genetic diversity.

Understanding global patterns of genetic diversity is essential for describing, monitoring, and preserving life on Earth. To date, efforts to map macrogenetic patterns have been restricted to vertebrates, which comprise only a small fraction of Earth's biodiversity. Here, we construct a global map of predicted insect mitochondrial genetic diversity from cytochrome c oxidase subunit 1 sequences, derived from open data. We calculate the mitochondrial genetic diversity mean and genetic diversity evenness of insect assemblages across the globe, identify their environmental correlates, and make predictions of mitochondrial genetic diversity levels in unsampled areas based on environmental data. Using a large single-locus genetic dataset of over 2 million globally distributed and georeferenced mtDNA sequences, we find that mitochondrial genetic diversity evenness follows a quadratic latitudinal gradient peaking in the subtropics. Both mitochondrial genetic diversity mean and evenness positively correlate with seasonally hot temperatures, as well as climate stability since the last glacial maximum. Our models explain 27.9% and 24.0% of the observed variation in mitochondrial genetic diversity mean and evenness in insects, respectively, making an important step towards understanding global biodiversity patterns in the most diverse animal taxon.

Limited, episodic diversification and contrasting phylogeography in a New Zealand cicada radiation.

BACKGROUND: The New Zealand (NZ) cicada fauna contains two co-distributed lineages that independently colonized the isolated continental fragment in the Miocene. One extensively studied lineage includes 90% of the extant species (Kikihia + Maoricicada + Rhodopsalta; ca 51 spp.), while the other contains just four extant species (Amphipsalta - 3 spp. + Notopsalta - 1 sp.) and has been little studied. We examined mitochondrial and nuclear-gene phylogenies and phylogeography, Bayesian relaxed-clock divergence timing (incorporating literature-based uncertainty of molecular clock estimates) and ecological niche models of the species from the smaller radiation. RESULTS: Mitochondrial and nuclear-gene trees supported the monophyly of Amphipsalta. Most interspecific diversification within Amphipsalta-Notopsalta occurred from the mid-Miocene to the Pliocene. However, interspecific divergence time estimates had large confidence intervals and were highly dependent on the assumed tree prior, and comparisons of uncorrected and patristic distances suggested difficulty in estimation of branch lengths. In contrast, intraspecific divergence times varied little across analyses, and all appear to have occurred during the Pleistocene. Two large-bodied forest taxa (A. cingulata, A. zelandica) showed minimal phylogeographic structure, with intraspecific diversification dating to ca. 0.16 and 0.37 Ma, respectively. Mid-Pleistocene-age phylogeographic structure was found within two smaller-bodied species (A. strepitans - 1.16 Ma, N. sericea - 1.36 Ma] inhabiting dry open habitats. Branches separating independently evolving species were long compared to intraspecific branches. Ecological niche models hindcast to the Last Glacial Maximum (LGM) matched expectations from the genetic datasets for A. zelandica and A. strepitans, suggesting that the range of A. zelandica was greatly reduced while A. strepitans refugia were more extensive. However, no LGM habitat could be reconstructed for A. cingulata and N. sericea, suggesting survival in microhabitats not detectable with our downscaled climate data. CONCLUSIONS: Unlike the large and continuous diversification exhibited by the Kikihia-Maoricicada-Rhodopsalta clade, the contemporaneous Amphipsalta-Notopsalta lineage contains four comparatively old (early branching) species that show only recent diversification. This indicates either a long period of stasis with no speciation, or one or more bouts of extinction that have pruned the radiation. Within Amphipsalta-Notopsalta, greater population structure is found in dry-open-habitat species versus forest specialists. We attribute this difference to the fact that NZ lowland forests were repeatedly reduced in extent during glacial periods, while steep, open habitats likely became more available during late Pleistocene uplift.

Reconciling phylogeography and ecological niche models for New Zealand beetles: Looking beyond glacial refugia.

Mitochondrial DNA (cox1) sequence data and recently developed coalescent phylogeography models were used to construct geo-spatial histories for the New Zealand fungus beetles Epistranus lawsoni and Pristoderus bakewelli (Zopheridae). These methods utilize continuous-time Markov chains and Bayesian stochastic search variable selection incorporated in BEAST to identify historical dispersal patterns via ancestral state reconstruction. Ecological niche models (ENMs) were incorporated to reconstruct the potential geographic distribution of each species during the Last Glacial Maximum (LGM). Coalescent analyses suggest a North Island origin for E. lawsoni, with gene flow predominately north-south between adjacent regions. ENMs for E. lawsoni indicated glacial refugia in coastal regions of both main islands, consistent with phylogenetic patterns but at odds with the coalescent dates, which implicate much older topographic events. Dispersal matrices revealed patterns of gene flow consistent with projected refugia, suggesting long-term South Island survival with population vicariance around the Southern Alps. Phylogeographic relationships are more ambiguous for P. bakewelli, although long-term survival on both main islands is evident. Divergence dates for both species are consistent with the topographic evolution of New Zealand over the last 10Ma, whereas the signature of the LGM is less apparent in the time-scaled phylogeny.

Identifying glacial refugia in a geographic parthenogen using palaeoclimate modelling and phylogeography: the New Zealand stick insect Argosarchus horridus (White).

We have used phylogeographic analysis of mitochondrial DNA (COI and COII genes) and ecological niche modelling (ENM) to reconstruct the population history of Argosarchus horridus (White), a widespread species of New Zealand stick insect. These data were used to address outstanding questions on the role of glacial refugia in determining the distribution and genetic structure of New Zealand species. Phylogeographic analysis shows a general pattern of high diversity in upper North Island and reduced diversity in lower North Island and South Island. The ENM indicates that during the last glacial maximum, A. horridus was largely restricted to refugia around coastal areas of North Island. The ENM also suggests refugia on the northeast coast of South Island and southeast coast of North Island and this prediction is verified by phylogeographic analysis, which shows a clade restricted to this region. Argosarchus horridus is also most likely a geographic parthenogen where males are much rarer at higher latitudes. The higher levels of genetic variation in northern, bisexual populations suggest southern and largely unisexual populations originated from southwardly expanding parthenogenetic lineages. Bayesian skyline analysis also provides support for a recent population size increase consistent with a large increase in geographic distribution in the late Pleistocene. These results exemplify the utility of integrating ENM and phylogeographic analysis in testing hypotheses on the origin of geographic parthenogenesis and effects of Pleistocene environmental change on biodiversity.

Phylogeography and ecological niche modelling implicate coastal refugia and trans-alpine dispersal of a New Zealand fungus beetle.

The Last Glacial Maximum (LGM) severely restricted forest ecosystems on New Zealand's South Island, but the extent of LGM distribution for forest species is still poorly understood. We used mitochondrial DNA phylogeography (COI) and ecological niche modelling (ENM) to identify LGM refugia for the mycophagous beetle Agyrtodes labralis (Leiodidae), a forest edge species widely distributed in the South Island. Both the phylogenetic analyses and the ENM indicate that A. labralis refuged in Kaikoura, Nelson, and along much of the South Island's west coast. Phylogeography of this species indicates that recolonization of the largely deforested east and southeast South Island occurred in a west-east direction, with populations moving through the Southern Alps, and that the northern refugia participated little in interglacial population expansion. This contradicts published studies of other New Zealand species, in which recolonization occurs in a north-south fashion from many of the same refugia.

Effects of volcanic ash on the forest canopy insects of Montserrat, West Indies.

The impact of ash deposition levels on canopy arthropods was studied on the West Indian island of Montserrat, the site of an ongoing volcanic eruption since 1995. Many of the island's natural habitats have been buried by volcanic debris, and remaining forests regularly receive volcanic ash deposition. To test the effect of ash on canopy arthropods, four study sites were sampled over a 15-mo period. Arthropod samples were obtained using canopy fogging, and ash samples were taken from leaf surfaces. Volcanic ash has had a significant negative impact on canopy arthropod populations, but the decline is not shared equally by all taxa present, and total population variation is within the variance attributed to other aboitic and biotic factors. The affected populations do not differ greatly from those of the neighboring island of St. Kitts, which has not been subject to recent volcanic activity. This indicates that observed effects on Montserrat's arthropod fauna have a short-term acute response to recent ash deposition rather than a chronic depression caused by repeated exposure to ash over the last decade.

An Anthropocene map of genetic diversity.

The Anthropocene is witnessing a loss of biodiversity, with well-documented declines in the diversity of ecosystems and species. For intraspecific genetic diversity, however, we lack even basic knowledge on its global distribution. We georeferenced 92,801 mitochondrial sequences for >4500 species of terrestrial mammals and amphibians, and found that genetic diversity is 27% higher in the tropics than in nontropical regions. Overall, habitats that are more affected by humans hold less genetic diversity than wilder regions, although results for mammals are sensitive to choice of genetic locus. Our study associates geographic coordinates with publicly available genetic sequences at a massive scale, yielding an opportunity to investigate both the drivers of this component of biodiversity and the genetic consequences of the anthropogenic modification of nature.

An horizon scan of biogeography.

The opportunity to reflect broadly on the accomplishments, prospects, and reach of a field may present itself relatively infrequently. Each biennial meeting of the International Biogeography Society showcases ideas solicited and developed largely during the preceding year, by individuals or teams from across the breadth of the discipline. Here, we highlight challenges, developments, and opportunities in biogeography from that biennial synthesis. We note the realized and potential impact of rapid data accumulation in several fields, a renaissance for inter-disciplinary research, the importance of recognizing the evolution-ecology continuum across spatial and temporal scales and at different taxonomic, phylogenetic and functional levels, and re-exploration of classical assumptions and hypotheses using new tools. However, advances are taxonomically and geographically biased, and key theoretical frameworks await tools to handle, or strategies to simplify, the biological complexity seen in empirical systems. Current threats to biodiversity require unprecedented integration of knowledge and development of predictive capacity that may enable biogeography to unite its descriptive and hypothetico-deductive branches and establish a greater role within and outside academia.

Concerted versus independent evolution and the search for multiple refugia: comparative phylogeography of four forest beetles.

Phylogeographic structure and its underlying causes are not necessarily shared among community members, with important implications for using individual organisms as indicators for ecosystem evolution, such as the identification of forest refugia. We used mitochondrial DNA (cox1), Bayesian coalescent ancestral state reconstruction (implemented in BEAST), and ecological niche models (ENMs) to construct geospatial histories for four codistributed New Zealand forest beetles (Leiodidae, Nitidulidae, Staphylinidae, and Zopheridae) to examine the extent to which they have tracked environmental changes together through time. Hindcast ENMs identified potential forest refugia during the Last Glacial Maximum, whereas ancestral state reconstruction identified key geographic connections for each species, facilitating direct comparison of dispersal patterns supported by the data and the time frame in which they occurred. Well-supported geographic state transitions for each species were mostly between neighboring regions, favoring a historical scenario of stepping stone colonization of newly suitable habitat rather than long distance dispersal. No geographic state transitions were shared by all four species, but three shared multiple projected South Island refugia and recent dispersal from the southernmost refugium. In contrast, strongly supported dispersal patterns in the refugia-rich northern South Island suggest more individualistic responses to environmental change in these ecologically similar forest species.