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.     

The impact of Quaternary Ice Ages on mammalian evolution

The Quaternary was a time of extensive evolution among mammals. Most living species arose at this time, and many of them show adaptations to peculiarly Quaternary environments. The latter include continental northern steppe and tundra, and the formation of lakes and offshore islands. Although some species evolved fixed adaptations to specialist habitats, others developed flexible adaptations enabling them to inhabit broad niches and to survive major environmental changes. Adaptation to short-term (migratory and seasonal) habitat change probably played a part in pre-adapting mammal species to the longer-term cyclical changes of the Quaternary. Fossil evidence indicates that environmental changes of the order of thousands of years have been sufficient to produce subspeciation, but speciation has typically required one hundred thousand to a few hundred thousand years, although there are both shorter and longer exceptions. The persistence of taxa in environments imposing strong selective regimes may have been important in forcing major adaptive change. Individual Milankovitch cycles are not necessarily implicated in this process, but nor did they generally inhibit evolutionary change among mammals: many evolutionary divergences built over multiple climatic cycles. Deduction of speciation timing requires input from fossils and modern phenotypic and breeding data, to complement and constrain mitochondrial DNA coalescence dates which appear commonly to overestimate taxic divergence dates and durations of speciation. Migrational and evolutionary responses to climate change are not mutually exclusive but, on the contrary, may be synergistic. Finally, preliminary analysis suggests that faunal turnover, including an important element of speciation, was elevated in the Quaternary compared with the Neogene, at least in some biomes. Macroevolutionary species selection or sorting has apparently resulted in a modern mammalian fauna enriched with fast-reproducing and/or adaptively generalist species.     

Explaining how and explaining why: developmental and evolutionary explanations of dominance

There have been two different schools of thought on the evolution of dominance. On the one hand, followers of Wright [Wright S. 1929. Am. Nat. 63: 274–279, Evolution: Selected Papers by Sewall Wright, University of Chicago Press, Chicago; 1934. Am. Nat. 68: 25–53, Evolution: Selected Papers by Sewall Wright, University of Chicago Press, Chicago; Haldane J.B.S. 1930. Am. Nat. 64: 87–90; 1939. J. Genet. 37: 365–374; Kacser H. and Burns J.A. 1981. Genetics 97: 639–666] have defended the view that dominance is a product of non-linearities in gene expression. On the other hand, followers of Fisher [Fisher R.A. 1928a. Am. Nat. 62: 15–126; 1928b. Am. Nat. 62: 571–574; Bürger R. 1983a. Math. Biosci. 67: 125–143; 1983b. J. Math. Biol. 16: 269–280; Wagner G. and Burger R. 1985. J. Theor. Biol. 113: 475–500; Mayo O. and Reinhard B. 1997. Biol. Rev. 72: 97–110] have argued that dominance evolved via selection on modifier genes. Some have called these “physiological” versus “selectionist,” or more recently [Falk R. 2001. Biol. Philos. 16: 285–323], “functional,” versus “structural” explanations of dominance. This paper argues, however, that one need not treat these explanations as exclusive. While one can disagree about the most likely evolutionary explanation of dominance, as Wright and Fisher did, offering a “physiological” or developmental explanation of dominance does not render dominance “epiphenomenal,” nor show that evolutionary considerations are irrelevant to the maintenance of dominance, as some [Kacser H. and Burns J.A. 1981. Genetics 97: 639–666] have argued. Recent work [Gilchrist M.A. and Nijhout H.F. 2001. Genetics 159: 423–432] illustrates how biological explanation is a multi-level task, requiring both a “top-down” approach to understanding how a pattern of inheritance or trait might be maintained in populations, as well as “bottom-up” modeling of the dynamics of gene expression.     

Several million years of stability among insect species because of,or in spite of,Ice Age climatic instability?

There is a curious paradox in the evolutionary legacy of Ice Ages. Studies of modern species suggest that they are currently evolving in response to changing environments. If extrapolated into the context of Quaternary Ice Ages, this evidence would suggest that the frequent climatic changes should have stimulated the evolutionary process and thus increased the rates of change within species and the number of speciation events. Extinction rates would, similarly, be high. Quaternary insect studies call into question these interpretations. They indicate that insect species show a remarkable degree of stability throughout the Ice Age climatic oscillations. The paradox arises from the apparent contradiction between abundant evidence of incipient speciation in insect populations at the present day and the evidence that, in the geological past, this apparently did not lead to sustained evolution.     

Temporal,spatial and ecological dynamics of speciation among amphi‐Beringian small mammals

Aim

Quaternary climate cycles played an important role in promoting diversification across the Northern Hemisphere, although details of the mechanisms driving evolutionary change are still poorly resolved. In a comparative phylogeographical framework, we investigate temporal, spatial and ecological components of evolution within a suite of Holarctic small mammals. We test a hypothesis of simultaneous divergence among multiple taxon pairs, investigating time to coalescence and demographic change for each taxon in response to a combination of climate and geography.

Location

Beringia, the nexus of the northern continents.

Methods

We used approximate Bayesian computation methods to test for simultaneous divergence among eight pairs of taxa, using cytochrome b gene sequences. We calculated coalescence times for eastern and western components of each pair and for the combined pairs, and relate dates to Quaternary climatic periodicity and combinations of environmental events and physical barriers. Population growth and expansion statistics were used to test evolutionary responses among taxa, including range shifts, persistence or periodic extirpation. Species distribution models (SDMs) for each taxon were used to predict their geographical ranges during the present interglacial, Last Glacial Maximum and previous interglacial.

Results

Multiple divergence events across Beringia were primarily coincident with extreme glacial cycles of the late Quaternary. Structure within Beringia is spatially consistent with at least three environmental barriers arising at different times: the Kolyma Uplands, Bering Strait and portions of the Bering Isthmus. Levels of divergence varied substantially, indicating evolutionary processes spanning deep and shallow time‐scales. The different demographics among taxa reflect their distinct ecological responses. SDMs predicted regional distributional changes through time and different spatial responses among taxa.

Main conclusions

Beringia predominantly constituted a dispersal corridor during the early Quaternary and a major centre of endemism in the late Quaternary. Coincident with severe glacial cycles, small mammal species were ‘caught’ in Beringia and diversified over multiple climatic phases. Relative genetic differentiation across Beringia appears to be related to ecological differences reflecting a gradual adaptation to Beringian environments through time. Some methodological constraints associated with resolving recent (late Quaternary) isolation events or drawing inferences from a single locus are discussed.     

The Ethical Basis for Sustainable Human Security: A Place for Anthropocentrism?

The deep and lasting changes to human behaviour that are required to address the global environmental crisis necessitate profound shifts in moral foundations. They amount to a change in what individuals and societies conceive of as progress. This imperative raises important questions about the justification, ends, and means of large-scale changes in people’s ethics. In this essay I will focus on the ends—the direction of moral change as prescribed by the goal of sustainable human flourishing. I shall present a meta-ethical critique of anthropocentrism and propose that only an ecocentric ethic can support the sustainable flourishing of humanity. This proposition does not necessarily contradict itself. My claim will be that the values subsumed under the broad concept of anthropocentrism are categorically counterproductive, informing an undesirable concept of “progress”. I support this claim with two lines of argument. On the one hand, the end values of anthropocentrism are shallow and the “flourishing of humanity” is ill-defined. The conceptual constraints of anthropocentrism itself preclude a more concise definition which would take into account the utter dependence of the flourishing of humanity on the health of ecological support structures. On the other hand, pursuing the values that inform the actions of anthropocentrists (which may be identical with the “flourishing of humanity”) leads to unintended and undesirable outcomes, even from the view of the anthropocentrist herself. Those problems are not encountered with an ecocentric ethic, and the conceptual steps necessary to adopt it are not insurmountable.     

On stratigraphic subdivision of hominoid fossil localities of Yuanmou,Yunnan

There are four hominoid localities in the Yuanmou basin. There is no appreciable difference of fossil mammals collected from them respectively. On the other hand, judging from the occurrence of the strata and the characteristics of the deposits as well as from the trace of the neotectonics, the “homo layers” are identical to “Ramapithecus layers” in their occurrence. Thus the Hominoid fossils are exactly the same age.     

The Origin of the Vertebrate Eye

In his considerations of “organs of extreme perfection,” Charles Darwin described the evidence that would be necessary to support the evolutionary origin of the eye, namely, demonstration of the existence of “numerous gradations” from the most primitive eye to the most perfect one, where each such tiny change had provided a survival advantage (however slight) to the organism possessing the subtly altered form. In this paper, we discuss evidence indicating that the vertebrate eye did indeed evolve through numerous subtle changes. The great majority of the gradual transitions that did occur have not been preserved to the present time, either in the fossil record or in extant species; yet clear evidence of their occurrence remains. We discuss the remarkable “eye” of the hagfish, which has features intermediate between a simple light detector and an image-forming camera-like eye and which may represent a step in the evolution of our eye that can now be studied by modern methods. We also describe the important clues to the evolutionary origin of the vertebrate eye that can be found by studying the embryological development of our own eye, by examining the molecular genetic record preserved in our own genes and in the genes of other vertebrates, and through consideration of the imperfections (or evolutionary “scars”) in the construction of our eye. Taking these findings together, it is possible to discuss in some detail how the vertebrate eye evolved.     

“Force-Talk” in Evolutionary Explanation: Metaphors and Misconceptions

The notion of “pressure” as an evolutionary “force” that “causes” evolution is a pervasive linguistic feature of biology textbooks, journal articles, and student explanatory discourse. We investigated the consequences of using a textbook and curriculum that incorporate so-called force-talk. We examined the frequency with which biology majors spontaneously used notions of evolutionary “pressures” in their explanations, students’ definitions and explanations of what they meant when they used pressures, and the structure of explanatory models that incorporated evolutionary pressures and forces. We found that 12–20 percent of undergraduates spontaneously used “pressures” and/or “forces” as explanatory factors but significantly more often in trait gain scenarios than in trait loss scenarios. The majority of explanations using “force-talk” were characterized by faulty evolutionary reasoning. We discuss the conceptual similarity between faulty notions of evolutionary pressures and linguists’ force-dynamic models of everyday reasoning and ultimately question the appropriateness of force-talk in evolution education.     

Linear-no-threshold is a radiation-protection standard rather than a mechanistic effect model

The linear-no-threshold (LNT) controversy covers much more than the mere discussion whether or not “the LNT hypothesis is valid”. It is shown that one cannot expect to find only one or even the only one dose–effect relationship. Each element within the biological reaction chain that is affected by ionizing radiation contributes in a specific way to the final biological endpoint of interest. The resulting dose–response relationship represents the superposition of all these effects. Till now there is neither a closed and clear picture of the entirety of radiation action for doses below some 10 mSv, nor does clear epidemiological evidence exist for an increase of risk for stochastic effects, in this dose range. On the other hand, radiation protection demands for quantitative risk estimates as well as for practicable dose concepts. In this respect, the LNT concept is preferred against any alternative concept. However, the LNT concept does not necessarily mean that the mechanism of cancer induction is intrinsically linear. It could hold even if the underlying multi-step mechanisms act in a non-linear way. In this case it would express a certain “attenuation” of non-linearities. Favouring LNT against threshold-, hyper-, or sub-linear models for radiation-protection purposes on the one hand, but preferring one of these models (e.g. for a specific effect) because of biological considerations for scientific purposes on the other hand, does not mean a contradiction.     

Genes versus phenotypes in the study of speciation

Despite persistent debate on the nature of species, the widespread adoption of Mayr’s biological species concept has led to a heavy emphasis on the importance of reproductive isolation to the speciation process. Equating the origin of species with the evolution of reproductive isolation has become common practice in the study of speciation, coincident with an increasing focus on elucidating the specific genetic changes (i.e.—speciation genes) underlying intrinsic reproductive barriers between species. In contrast, some have recognized that reproductive isolation is usually a signature effect rather than a primary cause of speciation. Here we describe a research paradigm that shifts emphasis from effects to causes in order to resolve this apparent contradiction and galvanize the study of speciation. We identify major elements necessary for a balanced and comprehensive investigation of the origin of species and place the study of so-called “speciation genes” into its appropriate context. We emphasize the importance of characterizing diverging phenotypes, identifying relevant evolutionary forces acting on those phenotypes and their role in the causal origins of reduced gene flow between incipient species, and the nature of the genetic and phenotypic boundaries that results from such processes. This approach has the potential to unify the field of speciation research, by allowing us to make better “historical” predictions about the fate of diverging populations regardless of taxon.     

Climate change in Europe and effects on thermal resources for crops

Atmospheric variables play a fundamental role in driving man-managed ecosystems and more specifically in agro-ecosystems, determining the quantity and quality of crop production. On the other hand, climate variability can be seen as the superimposition of gradual and abrupt changes. This paper is focused on European surface air temperature in the period 1951–2010. Analysis of this dataset identified breakpoints that define two homogeneous sub-periods: 1951–1987 and 1988–2010. Thermal resources for crops were analyzed adopting a “normal heat hours” approach. Computation highlighted a general increase in thermal resources in the European continent for crop groups II and III (C3 and C4 plants adapted to high or moderate temperatures), while a decline of thermal resources for crop group I (cold adapted C3) was highlighted in the Mediterranean area. The climate variability justifies a change in the potential latitudinal limits of different groups of crops, representing a fundamental step for crop adaptation to climate change.     

Coccolith evidence for Quaternary nutricline variations in the southern South China Sea

Nutricline variations during the last 1560 ka in the southern South China Sea are reconstructed using the relative abundance of the coccolithophore Florisphaera profunda in ODP Site 1143. Nutricline depth shows both long-term large magnitude variation and high frequency glacial–interglacial variation. On the long-term scale, the nutricline experienced four significant changes, which occurred at 900, 480, 250, and 50 ka respectively. According to these changes, five stages could be recognized during the last 1560 ka. From 1560 to 900 ka, the nutricline depth increased gradually. Around 900 ka, the nutricline abruptly shallowed and then remained stable until 480 ka. The nutricline was shallow during the time interval between 480 and 250 ka. At 250 ka, it deepened again and increased gradually until 50 ka. After 50 ka, the nutricline depth decreased gradually to modern values. On the glacial–interglacial scale, the variations in nutricline depth show different patterns before and after 900 ka. Before 900 ka, the nutricline was deep during glacial periods and shallow during interglacials. However, after 900 ka, the nutricline was deep during interglacials and shallow during glacials. Spectral analysis of the relative abundance of F. profunda shows a similar trend. In addition to the eccentricity (113, 76 ka), obliquity (55, 39 ka), and precession (24, 19 ka), we also find a 431 ka cycle. The former three periods reflect glacial–interglacial variations in nutricline, and the period of 431 ka reflects long-term variations in nutricline. We suggested that the variations in nutricline in the southern South China Sea were caused by global and regional climate changes. Glacial–interglacial variations in nutricline are mainly controlled by the East Asian monsoon, and the long-term variations might be related to the global climatic events, such as the mid-Pleistocene Revolution and the mid-Brunhes event.     

<Emphasis Type="Italic">Protungulatum</Emphasis>, Confirmed Cretaceous Occurrence of an Otherwise Paleocene Eutherian (Placental?) Mammal

Neither pre-Cenozoic crown eutherian mammals (placentals) nor archaic ungulates (“condylarths”) are known with certainty based on the fossil record. Herein we report a new species of the Paleocene archaic ungulate (“condylarth”) Protungulatum from undisputed Late Cretaceous aged rocks in Montana USA based on an isolated last upper premolar, indicating rare representatives of these common early Tertiary mammals appeared in North America a minimum of 300 k  years before the extinction of non-avian dinosaurs. The other 1200 mammal specimens from the locality are characteristic Late Cretaceous taxa. This discovery overturns the current hypothesis that archaic ungulates did not appear in North America until after the Cretaceous/Tertiary (K/T) boundary and also suggests that other reports of North American Late Cretaceous archaic ungulates may be correct. Recent studies, including ours, cannot determine whether Protungulatum does or does not belong to the crown clade Placentalia.     

Integrating environmental,molecular, and morphological data to unravel an ice‐age radiation of arctic‐alpine Campanula in western North America

Many arctic‐alpine plant genera have undergone speciation during the Quaternary. The bases for these radiations have been ascribed to geographic isolation, abiotic and biotic differences between populations, and/or hybridization and polyploidization. The Cordilleran Campanula L. (Campanulaceae Juss.), a monophyletic clade of mostly endemic arctic‐alpine taxa from western North America, experienced a recent and rapid radiation. We set out to unravel the factors that likely influenced speciation in this group. To do so, we integrated environmental, genetic, and morphological datasets, tested biogeographic hypotheses, and analyzed the potential consequences of the various factors on the evolutionary history of the clade. We created paleodistribution models to identify potential Pleistocene refugia for the clade and estimated niche space for individual taxa using geographic and climatic data. Using 11 nuclear loci, we reconstructed a species tree and tested biogeographic hypotheses derived from the paleodistribution models. Finally, we tested 28 morphological characters, including floral, vegetative, and seed characteristics, for their capacity to differentiate taxa. Our results show that the combined effect of Quaternary climatic variation, isolation among differing environments in the mountains in western North America, and biotic factors influencing floral morphology contributed to speciation in this group during the mid‐Pleistocene. Furthermore, our biogeographic analyses uncovered asynchronous consequences of interglacial and glacial periods for the timing of refugial isolation within the southern and northwestern mountains, respectively. These findings have broad implications for understanding the processes promoting speciation in arctic‐alpine plants and the rise of numerous endemic taxa across the region.     

Post-glacial redistribution and shifts in productivity of giant kelp forests

Quaternary glacial–interglacial cycles create lasting biogeographic, demographic and genetic effects on ecosystems, yet the ecological effects of ice ages on benthic marine communities are unknown. We analysed long-term datasets to develop a niche-based model of southern Californian giant kelp (Macrocystis pyrifera) forest distribution as a function of oceanography and geomorphology, and synthesized palaeo-oceanographic records to show that late Quaternary climate change probably drove high millennial variability in the distribution and productivity of this foundation species. Our predictions suggest that kelp forest biomass increased up to threefold from the glacial maximum to the mid-Holocene, then rapidly declined by 40–70 per cent to present levels. The peak in kelp forest productivity would have coincided with the earliest coastal archaeological sites in the New World. Similar late Quaternary changes in kelp forest distribution and productivity probably occurred in coastal upwelling systems along active continental margins worldwide, which would have resulted in complex shifts in the relative productivity of terrestrial and marine components of coastal ecosystems.     

The impact of early Quaternary climate change on the diversification and population dynamics of a South American cactus species

Aim

Climatic oscillations have been suggested to promote speciation and changes in species distributions, mostly in connection with the Last Glacial Maximum (LGM). However, the LGM is just the most recent of the 20+ glacial‐interglacial periods that characterise the Quaternary. Here, we investigate the role of climatic changes and geomorphological features in shaping the evolution, distribution and population dynamics of the South American cactus Cereus hildmannianus.

Location

South‐eastern South America.

Methods

We built a large fossil‐calibrated phylogeny for cacti (family Cactaceae), comprising 128 species distributed in all subfamilies, using a Bayesian relaxed clock. We used the results to derive a secondary calibration for a population‐level phylogeny in C. hildmannianus. We amplified two plastid (trnQ‐5′rps16 and psbJ‐petA) and one nuclear marker (PhyC) for 24 populations. We estimated population dynamics, ancestral areas, and species distribution models to infer the clade's evolutionary history in time and space.

Results

Our results show a major population divergence of C. hildmannianus at c. 2.60 Ma, which is strikingly coincident with the transition of the Pliocene–Pleistocene and onset of Quaternary glaciations. This was followed by a complex phylogeographic scenario involving population expansions across ecologically diverse regions.

Main conclusions

Contrary to the dominant research focus on the LGM, our study indicates a major impact of the first Quaternary glaciation on the distribution and population divergence of a South American plant species. Further intraspecific events seem related to successive climatic changes and geomorphology, including the development of the coastal plain and its peculiar diversity. We propose that the first Quaternary glaciation acted as a major evolutionary bottleneck, whereby many warm‐adapted lineages succumbed, while those that survived could diversify and better cope with subsequent climatic oscillations.     

Transforming Our Thinking about Transitional Forms

A common misconception of evolutionary biology is that it involves a search for “missing links” in the history of life. Relying on this misconception, antievolutionists present the supposed absence of transitional forms from the fossil record as evidence against evolution. Students of biology need to understand that evolution is a branching process, paleontologists do not expect to find “missing links,” and evolutionary research uses independent lines of evidence to test hypotheses and make conclusions about the history of life. Teachers can facilitate such learning by incorporating cladistics and tree-thinking into the curriculum and using evograms to focus on important evolutionary transitions.     

Evolutionary biology and feminism

Evolutionary biology and feminism share a variety of philosophical and practical concerns. I have tried to describe how a perspective from both evolutionary biology and feminism can accelerate the achievement of goals for both feminists and evolutionary biologists. In an early section of this paper I discuss the importance of variation to the disciplines of evolutionary biology and feminism. In the section entitled “Control of Female Reproduction” I demonstrate how insight provided by participation in life as woman and also as a feminist suggests testable hypotheses about the evolution of social behavior—hypotheses that are applicable to our investigations of the evolution of social behavior in nonhuman animals. In the section on “Deceit, Self-deception, and Patriarchal Reversals” I have overtly conceded that evolutionary biology, a scientific discipline, also represents a human cultural practice that, like other human cultural practices, may in parts and at times be characterized by deceit and self-deception. In the section on “Femininity” I have indicated how questions cast and answered and hypotheses tested from an evolutionary perspective can serve women and men struggling with sexist oppression. Patricia Adair Gowaty studies the evolution of social behavior, particularly mating systems and sex allocation, primarily in birds. She is most well-known for her long-term studies of eastern bluebirds, which began in 1977 and are on-going. She was an undergraduate at H. Sophie Newcomb College of Tulane University (1963–1967). In the late sixties and early seventies, while employed at the Bronx Zoo (New York Zoological Society), she belonged to a feminist “consciousness-raising” group. She started graduate school in 1974 at the University of Georgia and received her Ph.D. from Clemson University (1980). She had a postdoctoral position at the University of Oklahoma (1982–1983) and a visiting faculty position at Cornell University through the Visiting Professorships for Women NSF program (1983–1984) before returning to her bluebird study sites at Clemson in 1985. She has supported herself and her research efforts throughout her academic career on a series of awards and grants. She is currently (1990–1995) supported by a Research Scientist Development Award from The National Institute of Mental Health.