Quaternary Refugia Research Articles

Patterns of reef fish taxonomic and functional diversity in the Eastern Tropical Pacific

A core challenge in ecology is identifying the factors that determine species distribution and functional diversity of species assemblages. Reef fish are the most diverse group of vertebrates, form taxonomically rich and functionally diverse communities and represent a key source of food for humans. We examine regional distribution patterns of reef fish species richness and functional diversity and investigate how these are determined by historical, biogeographic, energetic, and anthropogenic factors. We compiled data from 3,312 underwater visual censuses performed at 122 locations comprising rocky and coral reefs along the Eastern Tropical Pacific (ETP). We used generalized linear mixed‐effects models (GLMMs) implemented in a Bayesian framework to investigate whether distance from quaternary refugia, distance from mainland, shelf area, primary productivity, sea surface temperature (SST), human population gravity, and conservation status influence reef fish species richness and functional diversity in the ETP. Species richness and functional richness (FRic) peaked towards the center of the ETP and our null model suggests that FRic followed a spatial pattern that would be predicted by species richness. Additionally, functional evenness (FEve) was highest at higher latitudes whereas functional dispersion (FDis) was homogeneous throughout the ETP. Species richness was negatively influenced by shelf area and distance from mainland, but positively influenced by SST and conservation status. FEve was influenced by human population gravity and FDis by shelf area. Reef fish species richness and functional diversity in the ETP exhibited a strong division within the region mainly mediated by SST and human population gravity. Our results also suggest that dominant species within small shelf areas share more common traits than dominant species in large areas. This study uncovers previously unknown regional patterns of reef fish functional diversity and provides new insights into how historical, biogeographic, energetic, and anthropogenic factors influence complementary biodiversity facets.

A trait‐based approach to marine island biogeography

AbstractAimThe Island Biogeography Theory (IBT) and its multiple extensions explain species diversity patterns in insular systems. However, how these theories can predict the functional diversity patterns in island systems remains challenging. Here, we evaluated the predictions of the IBT, the General Dynamic Theory of Oceanic Island Biogeography (GDM) and the Glacial‐sensitive model of Island Biogeography (GSM) considering the functional diversity of reef fishes on islands.LocationTropical oceanic islands.TaxonActinopterygii.MethodWe combined literature data and online repositories to gather occurrence data and traits of reef fish species for 72 tropical oceanic islands. We then calculated five functional diversity indices (functional richness ‘FRic’, functional evenness ‘FEve’, functional divergence ‘FDiv’, functional over‐redundancy ‘FOR’ and functional vulnerability ‘FVul’). We used generalized additive mixed models to explore relationships among species richness and functional indices. Furthermore, we built Bayesian models to evaluate relationships between the functional diversity indices and several island features (isolation from the nearest reef, past and present reef area, and geological age) and two metrics that reflect the potential influence of Quaternary climatic changes (isolation from Quaternary refugia) and historical contingency (isolation from biodiversity centres).ResultsWe observed higher levels of FRic, FDiv and FOR on the Indo‐Pacific islands, whereas FEve and FVul showed higher values on the Atlantic and Eastern Pacific islands. We identified positive relationships between FRic, FDiv and FOR with species richness but negative relationships with FEve and FVul. We found that past and present reef areas best explained the variation in functional diversity among islands.Main ConclusionsThe functional diversity of reef fishes on oceanic islands showed a longitudinal gradient, which can be explained by differences in the evolutionary history among marine regions. Furthermore, past and present reef areas were found to be the best predictors of reef fish functional diversity on oceanic islands, extending the IBT, GDM and GSM for marine organisms within a trait‐based framework.

Insights Into the Significance of the Chinense Loess Plateau for Preserving Biodiversity From the Phylogeography of Speranskia tuberculata (Euphorbiaceae).

The significance of the Chinese Loess Plateau (CLP) in maintaining biodiversity for northern China has rarely been shown, as previous phylogeographic studies are mostly woody species and they have revealed that Quaternary refugia are mainly located in mountain regions. We selected a drought-enduring endemic herb, Speranskia tuberculata (Euphorbiaceae), to determine its glacial refugia and postglacial demographic history. To this end, we sampled 423 individuals from 38 populations covering its entire geographic distribution. Three chloroplast DNA (cpDNA) fragments, two low-copy nuclear genes, and six nuclear microsatellites (nSSRs) were used and supplemented with ecological niche modeling (ENM) to infer the phylogeographic history of this species. Populations with private haplotypes and high haplotype diversity of cpDNA are mainly located in the CLP or scattered around northeastern China and the coastal region. Spatial expansion, detected using a neutrality test and mismatch distribution, may have resulted in a widely distributed ancestral cpDNA haplotype, especially outside of the CLP. For nuclear DNA, private haplotypes are also distributed mainly in the CLP. In nSSRs, STRUCTURE clustering identified two genetic clusters, which are distributed in the west (western cluster) and east (eastern cluster), respectively. Many populations belonged, with little to no admixture, to the western cluster while (hardly) pure populations of the eastern cluster were barely found. Genetic differentiation is significantly correlated with geographic distance, although genetic diversity is uniformly distributed. ENM suggests that the distribution of S. tuberculata has recently expanded northwards from the southern CLP, whereas it has experienced habitat loss in the south. Thus, S. tuberculata populations probably survived the last glacial maximum (LGM) in the southern CLP and experienced post-glacial expansion. Wind-dispersed pollen could bring the majority of genotypes to the front during spatial expansion, resulting in uniformly distributed genetic diversity. Based on evidence from molecular data and vegetation and climate changes since the LGM, we conclude that drought-enduring species, especially herbaceous species, are likely to have persisted in the CLP during the LGM and to have experienced expansion to other regions in northern China.

Temporal turnover of the flora of lake islands: The island of Lake Pamvotis (Epirus, Greece).

Lake Pamvotis is one of the Balkan "ancient" lakes, a Quaternary refugium of great environmental importance and ecological value, that is under various anthropogenic pressures. It belongs to a Natura 2000 Special Area for Conservation and Special Protection Area. Almost in the middle of the lake, there is an inhabited island - one of the two lake islands in Greece – that also attracts touristic interest. Τhe main objectives of the present study are to provide a floristic inventory of the protected island, combining data of two different sampling periods, within a 25 year interval, in order to estimate temporal beta diversity and species turnover of the island’s plant diversity. The value of the absolute and relative turnover rates of the floristic diversity of the island studied are 4.24 and 1.72, respectively and are amongst the higher rates reported for plants. The absolute difference between extinct (E) and immigrant (l) taxa is to a great extent accounted, concerning life forms, by therophytes (1.86), hemicryptophytes (1.56) and geophytes (1.04) and, for habitats, by taxa preferring agricultural and ruderal forms (2.52).

Quaternary refugia are associated with higher speciation rates in mammalian faunas of the Western Palaearctic

Quaternary climate changes have contributed to shape the biogeographic distribution of extant species. The combination of climatic niche conservatism and glacial‐interglacial cycles forced many species to retract their range limits for surviving under the advance of Pleistocene ice‐sheets. Refugia offered geographical opportunities for species to retreat, persist and, later on, begin recolonization processes under favourable environmental conditions. Here we explore the hypothesis that refugia have been not only crucial for the survival of multiple species but also acted as speciation centres for Western Palaearctic mammals. We define ‘recurrent massive refugia’ as those geographical regions that have historically accumulated the highest levels of co‐occurring species for several Quaternary cycles. Our assemblage‐level analyses identify the existence of refugia within the Iberian Peninsula and the Atlantic French margin that were recurrently selected by most mammals. The topographic heterogeneity, climatic stability and microhabitat availability of these refugial areas may have offered suitable habitat conditions for multiple species during different climatic events over time. Using a Bayesian analysis of macroevolutionary mixtures we detected that the higher level of divergence and accumulative evolutionary changes in mammals of the Western Palaearctic are found in refugia. The continuous retractions and expansions of species’ ranges during the Pleistocene promoted temporal changes in the composition and richness of communities in this biogeographic region. The reorganization of ecological composition driven by cyclical climatic events may have favoured the emergence of biotic interactions and ecological responses conducive to novel selective pressures. Our findings suggest, first, that multiple climatic changes in the form of glacial‐interglacial transitions during the Quaternary have left a detectable imprint on the observed geographical patterns of species richness in mammalian faunas of the Western Palaearctic, and second, highlight the importance of refugia for the preservation of species (‘museums’) and as centers of speciation and endemism (‘cradles’) as well.

Ecological divergence of two closely related Roscoea species associated with late Quaternary climate change

AbstractAimEcological differentiation of closely related species has attracted wide attention to explore its evolutionary significance in speciation. In particular, the prevalence of ecological speciation of sister species driven by Quaternary climate changes is debated. Here, we used two parapatric sister species, Roscoea humeana and R. cautleoides, to test whether ecological speciation was associated with Quaternary climate changes in these taxa.LocationHengduan‐Mountain Region (HMR), south‐west of China.MethodsNuclear ribosomal (ITS) and chloroplast DNA (cpDNA: psbA–trnH and trnL–trnF) were sequenced from 200 individuals. Gene genealogies were reconstructed using network, Bayesian inference and maximum likelihood methods. Interspecific divergence times were estimated with an isolation with migration model. Suitable habitats for each species were estimated with ecological niche modelling using Maxent and BIOCLIM. Niche overlap and niche divergence were tested using Schoener's D and Warren's I. Principal components analysis (PCA), multivariate analysis of variance (MANOVA) and discriminant function analysis (DFA) were also used to test ecological differentiation.ResultsGene genealogies indicated that the low‐elevational species R. cautleoides was derived from the high‐elevational species R. humeana. Divergence among species occurred during the middle to late Quaternary (0.01–1.48 Ma). The species distribution and phylogeographical pattern were inconsistent with a geographical barrier. Niche models and statistical analyses showed significant ecological differentiation.Main conclusionsDivergence between R. humeana and R. cautleoides was recent and coincident with Quaternary climate cycles. Ecological niche differentiation within Quaternary refugia may have promoted speciation.

Quaternary refugia and secondary contact in the southern boundary of the Brazilian subregion: comparative phylogeography of freshwater fish

Freshwater fish are an ideal model to illustrate how climate-tectonic changes affect the distribution of genetic variation. Freshwater bodies are extensively affected by environmental changes, with streams even changing their courses in the most extreme cases. Fortunately, this situation is reflected in the genetic composition of populations and may currently be inferred from the study of mitochondrial DNA molecular markers. Here we analyze and compare the phylogeographic patterns of the species Corydoras paleatus and Jenynsia multidentata at the southern limit of the Brazilian subregion. These basins are isolated in the current hydrogeographic pattern due to geologic and paleoclimatic changes. Our results support a concurrent pattern for both species. Some lineages have persisted in the area under adverse climate conditions, possibly in environmental refuges, while other lineages may have colonized the area later by means of paleodrainages connections. In addition, the presence of independent, greatly diverging lineages, even within the same watercourses, suggests secondary contact between these lineages. This work represents a first approach to understand how geologic and paleoclimatic changes have affected the distribution of genetic variation in the Southern Pampean Area.

Was Jeju Island a glacial refugium for East Asian warm‐temperate plants? Insights from the homosporous fern Selliguea hastata (Polypodiaceae)

We posed two hypotheses for broad scenarios of postglacial recolonization of Korea by the warm-temperate vegetation: (1) that extant Korean populations are derived from a single refugium, or (2) that they are derived from multiple refugia. We chose a homosporous fern typical of East Asian warm-temperate vegetation, Selliguea hastata, to test which of the two scenarios is more likely and to check whether Japan contained putative glacial refugia. Using 16 allozyme loci, we obtained genotypes of 756 individuals from 20 populations, representative of the whole distribution area in Korea (including Jeju Island), Japan, and Taiwan. We assessed genetic variability within and among populations, Wright's F-statistics, and conducted analysis of molecular variance, model-based Bayesian clustering, and bottleneck tests. We found no allozyme variation within populations of S. hastata in mainland Korea, whereas genetic polymorphism was detected for populations from Jeju Island, Japan (in particular a population from southeastern Shikoku), and Taiwan. The levels of inbreeding within populations were high, consistent with the potential of S. hastata for intragametophytic selfing. Data on allelic richness together with Bayesian clustering methods suggest a pattern of postglacial recolonization of mainland Korea from a single refugium, probably located either on Jeju Island or in Japan. Jeju Island should merit the highest priority for conservation biogeography, as it played a role as a Quaternary refugium for arctic-alpine, boreal, temperate as well as warm-temperate plants, as suggested here.

Quaternary refugia in southwestern Iran: insights from two sympatric moth species (Insecta, Lepidoptera)

Alternating glacial and interglacial periods led to range shifts (contractions and expansions), persistence in distinct glacial refugia and extinction events in various temperate organisms. Today, the integrative analysis of molecular markers and spatial distribution models conducted for multiple taxa allows the detection of phylogeographical patterns, thus reconstructing major biogeographical events in their shared evolutionary history. In this study, the effects of past climate change on the evolutionary history of two sympatric moth species (Gnopharmia colchidaria s.l. and G. kasrunensis) and their host plants (Prunus scoparia and P. fenzliana) were inferred for the largely neglected biodiversity hot spot Iran. We complementarily analyzed the population structure of both moth species (187 specimens, based on COI) in congruence with batched species distribution models (SDMs) for all four taxa and for the times of the Last Glacial Maximum (21 ky BP), 6 ky BP and today. Coincidence of SDMs and the distribution of haplotype lineages indicated a shared refugium for the southwestern Zagros Mountains and potential species-specific refugial areas in the southern Caucasus and the Kope-Dagh Mountains. Both moth species experienced past population expansion.

Chloroplast DNA phylogeography of the shrub Cistus ladanifer L. (Cistaceae) in the highly diverse Western Mediterranean region

This study investigated the phylogeographic structure of Cistus ladanifer, in order to locate its Quaternary refugia, reconstruct its recolonisation patterns and assess the role of geographical features (mountain ranges, rivers and the Strait of Gibraltar) as barriers to its seed flow and expansion through the Western Mediterranean. Thirty-eight populations were screened for length variation of polymorphic chloroplast simple sequence repeats (cpSSRs). Statistical analyses included estimation of haplotypic diversity, hierarchical analysis of molecular variation (amova) and fixation indices. Mantel tests, SAMOVA and BARRIER analyses were applied to evaluate the geographical partitioning of genetic diversity across the entire species range. Pollen data from bibliography were used to complement molecular inferences. Chlorotype diversity within populations was similar throughout the natural range of C. ladanifer (mean haplotypic diversity=0.32). High differentiation among populations was estimated (G(ST)=0.60). Our data suggest that the barriers of the Strait of Gibraltar and the Betic ranges may have favoured the divergence during glacial periods of four different lineages of populations inferred with SAMOVA. The main northward colonisation of in the Iberian Peninsula occurred from refugia in southwest Iberia. This process may have been influenced by human activities (forest clearance, livestock grazing and even commerce) in the Iberian Peninsula. In contrast, populations in the Betic area have conserved a specific haplotype.

ORIGIN, STATE AND PERSPECTIVES OF CHESTNUT CULTIVATION IN BULGARIA

The history of Castanea sativa Mill. (sweet chestnut) cultivation has been described on the basis of the available documentation. We have tried to identify the roles of the Greek and Roman civilizations in the dissemination of chestnut cultivation. This paper gives a short overview on the history and present situation of the chestnut cultivation in Bulgaria: presumed quaternary refugia, origin of the chestnut cultivation, driving factors of its diffusion. An attempt is made to describe the actual state of chestnut stands in the two significant regions in Bulgaria, the causes of the decline and future perspective of the European chestnut culture.

Mitochondrial DNA reveals complex genetic structuring in a stenoendemic conifer Picea omorika [(Panč.) Purk.] caused by its long persistence within the refugial Balkan region

Picea omorika (Panc.) Purk. is a relict from the Arcto-Tertiary flora with its entire current natural range confined to an area of only 10,000 km2 within the Balkans, a region well known as a Quaternary refugium. We have amplified the second intron of the mitochondrial NADH dehydrogenase subunit1 gene in 200 trees originating from ten natural populations to assess the phylogeographic structure and history of this conifer. Five haplotypes harbouring different numbers of 34-bp minisatellites were detected, revealing haplotypic richness of 3.007 and gene diversities HS = 0.075 and HT = 0.225. More interestingly, despite the very small distribution range of P. omorika and its dispersal by wind, non-random distribution of haplotypes was observed, resulting in an unexpectedly high estimate of population differentiation (GST = 0.668), and 56.8% of molecular variation assigned to variation among populations. Those findings suggest substantial isolation of populations and their partitioning into two gene pools characterized by different history and levels of genetic diversity, and very limited seed flow in this species (Nm = 0.25). They support the hypothesised early arrival of P. omorika in the Balkan region, and residence within this refugium during several ice ages at least. We demonstrate that the assessment of genetic diversity and structuring are not straightforward in species confined to refugial regions, and that past microvicariance might bias formal phylogeographic (GST = NST = 0.668) and isolation-by-distance analysis (r = 0.028, P > 0.05).

Eastern Asian endemic seed plant genera and their paleogeographic history throughout the Northern Hemisphere

AbstractWe review the fossil history of seed plant genera that are now endemic to eastern Asia. Although the majority of eastern Asian endemic genera have no known fossil record at all, 54 genera, or about 9%, are reliably known from the fossil record. Most of these are woody (with two exceptions), and most are today either broadly East Asian, or more specifically confined to Sino‐Japanese subcategory rather than being endemic to the Sino‐Himalayan area. Of the “eastern Asian endemic” genera so far known from the fossil record, the majority formerly occurred in Europe and/or North America, indicating that eastern Asia served as a late Tertiary or Quaternary refugium for taxa. Hence, many of these genera may have originated in other parts of the Northern Hemisphere and expanded their ranges across continents and former sea barriers when tectonic and climatic conditions allowed, leading to their arrival in eastern Asia. Although clear evidence for paleoendemism is provided by the gymnosperms Amentotaxus, Cathaya, Cephalotaxus, Cunninghamia, Cryptomeria, Glyptostrobus, Ginkgo, Keteleeria, Metasequoia, Nothotsuga, Pseudolarix, Sciadopitys, and Taiwania, and the angiosperms Cercidiphyllum, Choerospondias, Corylopsis, Craigia, Cyclocarya, Davidia, Dipelta, Decaisnea, Diplopanax, Dipteronia, Emmenopterys, Eucommia, Euscaphis, Hemiptelea, Hovenia, Koelreuteria, Paulownia, Phellodendron, Platycarya, Pteroceltis, Rehderodendron, Sargentodoxa, Schizophragma, Sinomenium, Tapiscia, Tetracentron, Toricellia, Trapella, and Trochodendron, we cannot rule out the possibility that neoendemism plays an important role especially for herbaceous taxa in the present‐day flora of Asia, particularly in the Sino‐Himalayan region. In addition to reviewing paleobotanical occurrences from the literature, we document newly recognized fossil occurrences that expand the geographic and stratigraphic ranges previously known for Dipelta, Pteroceltis, and Toricellia.

Conservation genetics of the endangered Iberian steppe plant Ferula loscosii (Apiaceae)

Ferula loscosii (Lange) Willk (Apiaceae) is a threatened endemic species native to the Iberian Peninsula. The plant has a narrow and disjunct distribution in three regions, NE, C and SE Spain. Genetic variability within and among 11 populations from its natural distribution was assessed using allozymes. Intermediate levels of genetic diversity were detected in F. loscosii (P(99%) = 36.83; H(E) = 0.125; H(T) = 0.152). However, the highest genetic diversity (58%) corresponded to the threatened populations from SE and C Spain (H(T) = 0.169) rather than the more abundant and larger populations from NE Spain (Ebro valley) (H(T) = 0.122). Low to moderate levels of genetic structure were found among regional ranges (G(ST) = 0.134), and several statistical spatial correlation analyses corroborated substantial genetic differentiation among the three main regional ranges. However, no significant genetic differentiation was found among the NE Spain populations, except for a northernmost population that is geographically isolated. Outcrossing mating and other biological traits of the species could account for the maintenance of the present values of genetic diversity within populations. The existence of an ancestral late Tertiary wider distribution of the species in SE and C Spain, followed by the maintenance of different Quaternary refugia in these warmer areas, together with a more recent and rapid post-glacial expansion towards NE Spain, are arguments that could explain the low genetic variability and structure found in the Ebro valley and the higher levels of diversity in the southern Iberian populations.

Response to Comment on "Buffered Tree Population Changes in a Quaternary Refugium: Evolutionary Implications"

Stewart reiterates recently published views on the possible existence of “cryptic” refugia in northern Europe and questions the role of southern European refugia as centers for speciation. In view of the implications of these issues for conservation strategies, critical evaluation of the genetic and paleobotanical evidence is particularly important.

Buffered tree population changes in a quaternary refugium: evolutionary implications.

A high-resolution pollen record from western Greece shows that the amplitude of millennial-scale oscillations in tree abundance during the last glacial period was subdued, with temperate tree populations surviving throughout the interval. This provides evidence for the existence of an area of relative ecological stability, reflecting the influence of continued moisture availability and varied topography. Long-term buffering of populations from climatic extremes, together with genetic isolation at such refugial sites, may have allowed lineage divergence to proceed through the Quaternary. Such ecologically stable areas may be critical not only for the long-term survival of species, but also for the emergence of new ones.

The late Quaternary environmental history of Bátorliget, N.E. Hungary

A sedimentary sequence extending back into the last glacial has been obtained from Bátorliget marsh in N.E. Hungary. Reconstruction of the environmental history of the region using the techniques of pollen analysis, molluscan analysis and geochemistry has revealed an important late Quaternary refugium. During the last glacial, a refugium for temperate flora and fauna existed within a landscape dominated by coniferous forest predominantly made up of Pinus and Picea. The lateglacial/postglacial transition at 10,000 yr B.P. resulted in a dramatic shift from coniferous (but also including Betula) woodland to deciduous woodland. Following the lateglacial/postglacial transition, a highly diverse woodland became established in the early postglacial, accompanied by an equally diverse molluscan assemblage. This diversity remained throughout the early postglacial although the types present within the woodland changed a number of times. At c. 7000 yr B.P. anthropogenic disturbance resulted in the destruction of the mixed forest and the development of agricultural land. The importance of this region as a refugial area both in the lateglacial and early postglacial is discussed and the influence that it had on the postglacial development of the fauna and flora of northeastern Hungary is reviewed.