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Keywords:

  • climatic shift;
  • devolution;
  • embryonic abortion;
  • genetic variation;
  • habitat attenuation;
  • habitat dissolution;
  • heterosis;
  • negative selection;
  • norm of reaction;
  • reproductive fitness

Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. THE ROLE OF EXTINCTION IN BIOHISTORY
  5. THE LINGUISTICS OF EXTINCTION: VOCABULARY, USAGE, SEMANTICS
  6. DEVOLUTION: A WORD TO DESCRIBE THE PROCESS OF BACKGROUND EXTINCTION
  7. BACKGROUND EXTINCTION AS A PROCESS
  8. CLARIFYING THE ISSUE OF EXTINCTION CAUSE
  9. THE MECHANISM OF BACKGROUND EXTINCTION
  10. THE LOSS OF REPRODUCTIVE FITNESS AND EXTINCTION: A THEOREM TOO SIMPLE?
  11. WHY REPRODUCTIVE FITNESS HAS BEEN NEGLECTED AS THE MECHANISM OF BACKGROUND EXTINCTION
  12. CAN THERE BE SELECTION AGAINST REPRODUCTION?
  13. EXTINCTION AMONG SHORT-LIVED SPECIES
  14. LINKING PROXIMATE AND ULTIMATE CAUSES OF BACKGROUND EXTINCTION: REPRODUCTIVE FITNESS AND NORM OF REACTION
  15. NATURAL SELECTION AND BACKGROUND EXTINCTION
  16. THE INCIDENCE OF BACKGROUND EXTINCTION
  17. CLIMATIC SHIFT AND BACKGROUND EXTINCTION
  18. BIOLOGICAL FACTORS AND EXTINCTION
  19. PHASES OF BACKGROUND EXTINCTION: HABITAT ATTENUATION AND DISSOLUTION
  20. CONCLUSIONS
  21. ACKNOWLEDGEMENTS
  22. REFERENCES

Following publication of On the Origin of Species, biologists concentrated on and resolved the mechanisms of adaptation and speciation, but largely ignored extinction. Thus, extinction remained essentially a discipline of palaeontology. Adequate language is not available to describe extinction phenomena because they must be discussed in the passive voice, wherein populations simply ‘go extinct’ without reference to process, specifics, effects, or causality. Extinction is also described typically in terms of its dynamics (including rate or risk), and although correlative variables enhance our ability to predict extinction, they do not necessarily enable an understanding of process. Yet background extinction, like evolution, is a process requiring a functional explanation, without which it is impossible to formulate mechanisms. We define the mechanism of background extinction as a typically long-term, multi-generational loss of reproductive fitness. This simple concept has received little credence because of a perception that excess generation of progeny ensures population sustainability, and perhaps the misconception that the loss of reproductive fitness somehow constitutes selection against reproduction itself. During environmental shifts, reproductive fitness is compromised when biotic or abiotic extremes consistently exceed existing norms of reaction. Subsequent selection will now favour individual survival over reproductive fitness, initiating long-term negative selection pressure and population decline. Background extinction consists typically of two intergrading phases: habitat attenuation and habitat dissolution. These processes generate the relict populations that characterize many species undergoing background extinction. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105, 255–268.


INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. THE ROLE OF EXTINCTION IN BIOHISTORY
  5. THE LINGUISTICS OF EXTINCTION: VOCABULARY, USAGE, SEMANTICS
  6. DEVOLUTION: A WORD TO DESCRIBE THE PROCESS OF BACKGROUND EXTINCTION
  7. BACKGROUND EXTINCTION AS A PROCESS
  8. CLARIFYING THE ISSUE OF EXTINCTION CAUSE
  9. THE MECHANISM OF BACKGROUND EXTINCTION
  10. THE LOSS OF REPRODUCTIVE FITNESS AND EXTINCTION: A THEOREM TOO SIMPLE?
  11. WHY REPRODUCTIVE FITNESS HAS BEEN NEGLECTED AS THE MECHANISM OF BACKGROUND EXTINCTION
  12. CAN THERE BE SELECTION AGAINST REPRODUCTION?
  13. EXTINCTION AMONG SHORT-LIVED SPECIES
  14. LINKING PROXIMATE AND ULTIMATE CAUSES OF BACKGROUND EXTINCTION: REPRODUCTIVE FITNESS AND NORM OF REACTION
  15. NATURAL SELECTION AND BACKGROUND EXTINCTION
  16. THE INCIDENCE OF BACKGROUND EXTINCTION
  17. CLIMATIC SHIFT AND BACKGROUND EXTINCTION
  18. BIOLOGICAL FACTORS AND EXTINCTION
  19. PHASES OF BACKGROUND EXTINCTION: HABITAT ATTENUATION AND DISSOLUTION
  20. CONCLUSIONS
  21. ACKNOWLEDGEMENTS
  22. REFERENCES

Evolution was conceived by Darwin and Wallace as a positive, creative process leading to adaptation and speciation through the mechanism of natural selection. This concept of evolution remains essentially unaltered in contemporary biological thought. In contrast, extinction is a negative, retrogressive process leading to population and species demise. Whereas the mechanisms of evolution are now relatively well known, there is little empirical evidence relating to the processes and mechanisms of background extinction (those not associated with catastrophic or mass extinctions), and there is no comprehensive theory that characterizes extinction (Caughley, 1994). This disparity of knowledge between evolution and extinction is readily demonstrable by comparing the space devoted to each topic in contemporary biological and evolutionary texts. [We are acutely aware of the much-publicized extinction crisis resulting from extirpation, i.e. human-mediated ecosystem disruption and hunting over-kill (Wilson, 2002; Thomas et al., 2004; Barnosky et al., 2011). However, we consider this crisis largely a social problem, not as a complex scientific question.] We posit that little more is understood about the specifics and empirical mechanisms of background extinction than were known to Darwin and Wallace!

Darwin (1859) noted that ‘the appearance of new forms and disappearance of old are bound together’, an observation based upon observations of the fossil record, which revealed that large extinction events had been accompanied by rapid evolution. Observation of extinction in the 19th century was primarily limited to large-scale past events on geological time scales, using a body of evidence that concentrated on correlation between events (e.g. extinction and evolution), more so than determination of process and mechanism. The paucity of long-term observation of living populations in decline was undoubtedly a factor in the absence of further investigation into the mechanism of decline. Similarly, a limited knowledge base of species niches made the causes of population fluctuation difficult to determine.

Darwin commented, ‘We need not marvel at extinction’, but instead should focus on the ‘many complex contingencies on which the existence of each species depends’. Darwin recognized the necessity that biologists delve deeply into the empirical work of physiology and ecology before drawing conclusions about extinction.

The purpose of this study is to review the reasons why the modes of extinction have received so little attention from the biological community over the past 150 years and to propose a mechanism for the process of background extinction.

THE ROLE OF EXTINCTION IN BIOHISTORY

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. THE ROLE OF EXTINCTION IN BIOHISTORY
  5. THE LINGUISTICS OF EXTINCTION: VOCABULARY, USAGE, SEMANTICS
  6. DEVOLUTION: A WORD TO DESCRIBE THE PROCESS OF BACKGROUND EXTINCTION
  7. BACKGROUND EXTINCTION AS A PROCESS
  8. CLARIFYING THE ISSUE OF EXTINCTION CAUSE
  9. THE MECHANISM OF BACKGROUND EXTINCTION
  10. THE LOSS OF REPRODUCTIVE FITNESS AND EXTINCTION: A THEOREM TOO SIMPLE?
  11. WHY REPRODUCTIVE FITNESS HAS BEEN NEGLECTED AS THE MECHANISM OF BACKGROUND EXTINCTION
  12. CAN THERE BE SELECTION AGAINST REPRODUCTION?
  13. EXTINCTION AMONG SHORT-LIVED SPECIES
  14. LINKING PROXIMATE AND ULTIMATE CAUSES OF BACKGROUND EXTINCTION: REPRODUCTIVE FITNESS AND NORM OF REACTION
  15. NATURAL SELECTION AND BACKGROUND EXTINCTION
  16. THE INCIDENCE OF BACKGROUND EXTINCTION
  17. CLIMATIC SHIFT AND BACKGROUND EXTINCTION
  18. BIOLOGICAL FACTORS AND EXTINCTION
  19. PHASES OF BACKGROUND EXTINCTION: HABITAT ATTENUATION AND DISSOLUTION
  20. CONCLUSIONS
  21. ACKNOWLEDGEMENTS
  22. REFERENCES

There is general agreement that about 99.9% or more of all species that ever existed are now extinct (Raup, 1991). Therefore, it must follow that evolution and extinction are of approximately equal importance and together constitute the fundamental dichotomy in biohistory (Simpson, 1953; Dobzhansky, 1968). For more than half a century, eminent evolutionary biologists have opined over our lack of information relating to the details and mechanisms of background extinction. Extinction has been considered ‘a very complex problem’ (Huxley, Hardy & Ford, 1954), that ‘… astonishingly little is known about its precise causes’ (MacArthur, 1972), or ‘… the causes of extinction are so complex as to defy discovery …’ (Ayala & Valentine, 1979), and ‘… little is known of its specific causes’ (Futuyma, 2009). Perhaps Gould (1991) aptly summarized the situation with his wry comment that extinction should be acknowledged, but ‘not intensely discussed in polite company’.

Is Gould's comment simply a fanciful statement regarding biologists' view of extinction, or does it reflect a pervasive attitude in western society that emphasizes optimism and attention to the positive? Has such sentiment also unintentionally prejudiced biologists against the study of extinction? Fortey (1998) suggests that extinction is generally entwined with the idea of punishment for inadequacy, e.g. ‘Industrial dinosaurs are doomed to extinction’. Neglecting the possibility of failure, while remaining fettered by optimism, has had powerful ramifications in society as a whole, in both socio-economic and scientific areas (Ehrenreich, 2009).

We posit that the mechanism of background extinction has remained unresolved, not because its causes are unknowable or because of its complexity, but rather because of the mind-set that has characterized our thinking about the problem. The absence of language to discuss extinction phenomena adequately has resulted in a general failure to recognize extinction as a process.

THE LINGUISTICS OF EXTINCTION: VOCABULARY, USAGE, SEMANTICS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. THE ROLE OF EXTINCTION IN BIOHISTORY
  5. THE LINGUISTICS OF EXTINCTION: VOCABULARY, USAGE, SEMANTICS
  6. DEVOLUTION: A WORD TO DESCRIBE THE PROCESS OF BACKGROUND EXTINCTION
  7. BACKGROUND EXTINCTION AS A PROCESS
  8. CLARIFYING THE ISSUE OF EXTINCTION CAUSE
  9. THE MECHANISM OF BACKGROUND EXTINCTION
  10. THE LOSS OF REPRODUCTIVE FITNESS AND EXTINCTION: A THEOREM TOO SIMPLE?
  11. WHY REPRODUCTIVE FITNESS HAS BEEN NEGLECTED AS THE MECHANISM OF BACKGROUND EXTINCTION
  12. CAN THERE BE SELECTION AGAINST REPRODUCTION?
  13. EXTINCTION AMONG SHORT-LIVED SPECIES
  14. LINKING PROXIMATE AND ULTIMATE CAUSES OF BACKGROUND EXTINCTION: REPRODUCTIVE FITNESS AND NORM OF REACTION
  15. NATURAL SELECTION AND BACKGROUND EXTINCTION
  16. THE INCIDENCE OF BACKGROUND EXTINCTION
  17. CLIMATIC SHIFT AND BACKGROUND EXTINCTION
  18. BIOLOGICAL FACTORS AND EXTINCTION
  19. PHASES OF BACKGROUND EXTINCTION: HABITAT ATTENUATION AND DISSOLUTION
  20. CONCLUSIONS
  21. ACKNOWLEDGEMENTS
  22. REFERENCES

‘… most errors result solely from the incorrect application of words …’ (Spinoza, 1677).

Language communicates essential facts about the environment relevant to our well-being and even survival. It also influences cognitive processes; as Burke (2003) points out, ‘language does our thinking’. If this is correct, cognition requires appropriate vocabulary to formulate ideas and concepts.

We should therefore not find it surprising that there is inadequate terminology to explain extinction phenomena. For example, we often comment on the ability ‘to evolve’, ‘evolvability’, or ‘evolutionism’, but not ‘to extinct’, ‘extinctability’, or ‘extinctionism’. Likewise, there are ‘evolutionists’, but no ‘extinctionists’. Although ‘evolve’ is a verb, ‘extinct’ is an adjective (Raup, 1991); however, ‘extinct’ is not an adjective with the descriptive power of ‘evolutionary’. Thus, we can readily relate to the phrase ‘an evolutionary explanation’, but not to ‘an extinctionary explanation’. These linguistic difficulties manifest themselves when attempting to define extinction, leading to such phrases as ‘extinction is caused by the failure to adapt’, or ‘species become extinct because they no longer evolve’. Such expressions are essentially tautological (Raup, 1984) and simply beg the question of process and mechanism.

These problems of language seem largely attributable to the absence of a verb for extinction that expresses both process and action. As Raup (1991) comments, without a verb, references to extinction must be expressed in the passive voice. Thus, populations commonly ‘evolve’ (intimating the processes of adaptation and speciation), but populations can only ‘go’ or ‘become’ extinct. Consequently, extinction becomes a mere result without reference to process, specifics, or mechanism. In such a conceptual framework, the agents of causality are omitted. The result is a lack of accountability within the population that has gone extinct and de-emphasis of the processes that led to population demise. Finally, in the passive voice, extinction can only refer to something that has occurred in the past, thus intimating (unwittingly) that extinction is not an ongoing process.

These considerations may seem trivial, but linguists are in agreement that such usage not only influences our thinking ‘… but are all the more powerful for their subtlety; i.e. the reader is often unaware of how controlling these forces may be, since only rarely is the reader consciously noting distinctions between parts of speech’ (Gopen, 2004). In this way, language has indirectly influenced our understanding of causality in relation to extinction.

Further exacerbating the language problem and the mind-set surrounding the concept of extinction was the assumption that extinction (sensu Darwin) was simply a necessary side effect of evolution that occurred as a result of competition in resource-limited environments. Such an assumption is analogous to the linguistic obstacles that impeded the description of extinction phenomena and undoubtedly reinforced the idea that extinction was only a facet of evolution and thus required no further elaboration.

If indeed language does our thinking, it also enables and abets the possibility of not thinking. Thus, inadequate vocabulary and the notion that extinction was only an aspect of evolution may not only have impeded, but also effaced from our consciousness, the idea that extinction is a process and that evolution and extinction are of equal importance in biohistory. We stress that these difficulties are only an unfortunate caprice of language and mind-set that have largely silenced our thinking about the processes and mechanism of extinction.

DEVOLUTION: A WORD TO DESCRIBE THE PROCESS OF BACKGROUND EXTINCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. THE ROLE OF EXTINCTION IN BIOHISTORY
  5. THE LINGUISTICS OF EXTINCTION: VOCABULARY, USAGE, SEMANTICS
  6. DEVOLUTION: A WORD TO DESCRIBE THE PROCESS OF BACKGROUND EXTINCTION
  7. BACKGROUND EXTINCTION AS A PROCESS
  8. CLARIFYING THE ISSUE OF EXTINCTION CAUSE
  9. THE MECHANISM OF BACKGROUND EXTINCTION
  10. THE LOSS OF REPRODUCTIVE FITNESS AND EXTINCTION: A THEOREM TOO SIMPLE?
  11. WHY REPRODUCTIVE FITNESS HAS BEEN NEGLECTED AS THE MECHANISM OF BACKGROUND EXTINCTION
  12. CAN THERE BE SELECTION AGAINST REPRODUCTION?
  13. EXTINCTION AMONG SHORT-LIVED SPECIES
  14. LINKING PROXIMATE AND ULTIMATE CAUSES OF BACKGROUND EXTINCTION: REPRODUCTIVE FITNESS AND NORM OF REACTION
  15. NATURAL SELECTION AND BACKGROUND EXTINCTION
  16. THE INCIDENCE OF BACKGROUND EXTINCTION
  17. CLIMATIC SHIFT AND BACKGROUND EXTINCTION
  18. BIOLOGICAL FACTORS AND EXTINCTION
  19. PHASES OF BACKGROUND EXTINCTION: HABITAT ATTENUATION AND DISSOLUTION
  20. CONCLUSIONS
  21. ACKNOWLEDGEMENTS
  22. REFERENCES

Evolution was verbalized by the mid 17th century from the Latin ‘evolvere’ (to unroll or unfold), but there is presently no equivalent verb form for extinction, even though it was derived from the Latin verb ‘extinguere’ (to extinguish) in the late 14th century. To resolve the difficulties previously discussed, we require an antonym for evolution with a verb form that imparts not only a sense of process, but also produces an opposing result (extinction). For such an antonym we suggest the noun ‘devolution’ and verb ‘to devolve’. Thus, devolution results in population decline and extinction, whereas evolution results in adaptation and speciation, as well as potential population growth.

Devolution, from the Latin ‘devolutio’ (to roll or descend downward), and its infinitive, to devolve, from the Latin ‘devolvere’ (to transfer or pass on), have a history of use from the 14th century in law, politics, and religion, where they generally denote a descending series of transference or succession. However, devolution is rarely mentioned in biological discourse, where it signifies retrogression, degeneration, or simplification of structures, and in this context we have encountered its use in print only once (Barlow, 2000). Unfortunately, devolution has been used in the anti-evolution literature, a subject not pertinent to the present study.

BACKGROUND EXTINCTION AS A PROCESS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. THE ROLE OF EXTINCTION IN BIOHISTORY
  5. THE LINGUISTICS OF EXTINCTION: VOCABULARY, USAGE, SEMANTICS
  6. DEVOLUTION: A WORD TO DESCRIBE THE PROCESS OF BACKGROUND EXTINCTION
  7. BACKGROUND EXTINCTION AS A PROCESS
  8. CLARIFYING THE ISSUE OF EXTINCTION CAUSE
  9. THE MECHANISM OF BACKGROUND EXTINCTION
  10. THE LOSS OF REPRODUCTIVE FITNESS AND EXTINCTION: A THEOREM TOO SIMPLE?
  11. WHY REPRODUCTIVE FITNESS HAS BEEN NEGLECTED AS THE MECHANISM OF BACKGROUND EXTINCTION
  12. CAN THERE BE SELECTION AGAINST REPRODUCTION?
  13. EXTINCTION AMONG SHORT-LIVED SPECIES
  14. LINKING PROXIMATE AND ULTIMATE CAUSES OF BACKGROUND EXTINCTION: REPRODUCTIVE FITNESS AND NORM OF REACTION
  15. NATURAL SELECTION AND BACKGROUND EXTINCTION
  16. THE INCIDENCE OF BACKGROUND EXTINCTION
  17. CLIMATIC SHIFT AND BACKGROUND EXTINCTION
  18. BIOLOGICAL FACTORS AND EXTINCTION
  19. PHASES OF BACKGROUND EXTINCTION: HABITAT ATTENUATION AND DISSOLUTION
  20. CONCLUSIONS
  21. ACKNOWLEDGEMENTS
  22. REFERENCES

Process is a series of actions, changes, events, or functions that require time and produce a result or effect. We stress the importance of this point, for if we ignore that background extinction is a process that requires both linear time (in geological context), as well as biological time that also has a cyclical component (measured in generations), there can be no effect. Without an understanding of both proximate cause and ultimate effect, it seems impossible to establish mechanisms. Furthermore, causes may be multiple, synergistic, or otherwise inter-related. Yet we are aware of only a few instances in which extinction is referred to as a process (Raup, 1984; Gilpin & Soulé, 1986; Jablonski, 1986; Levinton, 1988).

There is a continuum between catastrophic, mass, and background extinctions. Catastrophic extinction is stochastic and rapid (probably occurring within the maximum lifespan of the species), and neither genotype, fecundity, age, nor any aspect of organismal viability is generally relevant to survival. Mass extinctions occur at relatively high rates over a relatively short period of geological time. These are spectacular events in biohistory and have received a great deal of attention by palaeontologists. However, they account for only ∼ 5% of all extinctions (Raup, 1994). Background extinction is a multi-generational, devolutionary process and accounts for the vast majority of all extinctions. Extinctions may occur anywhere along this continuum; however, all extinctions beyond catastrophe require some degree of devolutionary process.

The importance of catastrophism, in contrast to gradualism, was described by Raup (1986) as the Lyell–Cuvier debate that has been periodically revived over the last 150 years. This debate was initiated by Lyell's sharp rejection of Cuvier's description of sudden catastrophic extinctions, and emphasized the overarching importance of slow and regular geological causes. While our review may be regarded as a continuation of that debate, we hope to make a clear distinction between cause and process.

CLARIFYING THE ISSUE OF EXTINCTION CAUSE

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. THE ROLE OF EXTINCTION IN BIOHISTORY
  5. THE LINGUISTICS OF EXTINCTION: VOCABULARY, USAGE, SEMANTICS
  6. DEVOLUTION: A WORD TO DESCRIBE THE PROCESS OF BACKGROUND EXTINCTION
  7. BACKGROUND EXTINCTION AS A PROCESS
  8. CLARIFYING THE ISSUE OF EXTINCTION CAUSE
  9. THE MECHANISM OF BACKGROUND EXTINCTION
  10. THE LOSS OF REPRODUCTIVE FITNESS AND EXTINCTION: A THEOREM TOO SIMPLE?
  11. WHY REPRODUCTIVE FITNESS HAS BEEN NEGLECTED AS THE MECHANISM OF BACKGROUND EXTINCTION
  12. CAN THERE BE SELECTION AGAINST REPRODUCTION?
  13. EXTINCTION AMONG SHORT-LIVED SPECIES
  14. LINKING PROXIMATE AND ULTIMATE CAUSES OF BACKGROUND EXTINCTION: REPRODUCTIVE FITNESS AND NORM OF REACTION
  15. NATURAL SELECTION AND BACKGROUND EXTINCTION
  16. THE INCIDENCE OF BACKGROUND EXTINCTION
  17. CLIMATIC SHIFT AND BACKGROUND EXTINCTION
  18. BIOLOGICAL FACTORS AND EXTINCTION
  19. PHASES OF BACKGROUND EXTINCTION: HABITAT ATTENUATION AND DISSOLUTION
  20. CONCLUSIONS
  21. ACKNOWLEDGEMENTS
  22. REFERENCES

Cause(s) are extensively used in statements regarding extinction by both palaeontologists and biologists, but process (devolution) and effect are rarely mentioned. We suspect that the extensive attention given to catastrophic and mass extinctions, especially the end-Cretaceous asteroid impact (Raup, 1986), has played a subconscious role in focusing our concepts of extinction into ‘single-cause/catastrophic’ modes of thinking.

Cause-alone reasoning may, at least in part, have originated from the observation of catastrophic events in which the time interval between cause and effect is so close that virtually all aspects of population death are immediately obvious. Thus, if a lava stream obliterates a population, cause (lethal temperatures) and the immediate effect (incineration) are clear. However, the longer and more complex the causal chain, the greater is the difficulty in establishing the relationship between initial cause and final effect (Mayr, 1988).

We also suggest that because of the intense focus on the cause(s) of extinction, especially catastrophic/mass extinctions, the definition of cause has been gradually (if unintentionally) distorted and broadened from its basic definition of an event that produces a result into a meaning that is inclusive of effect (Caughley, 1994). By treating effects as causes, the necessity of thinking in terms of devolutionary processes is circumvented. Such a semantic alteration not only obfuscates the distinction between the terms, it also has the potential of transforming the meaning of cause into the broader concept of causality, or the relationship between original cause and ultimate effect. Finally, in cases where more precise determination of causes are apparent, e.g. the end-Cretaceous extinction or contemporary habitat loss, we pose the question of whether there has been a tendency to consider the cause itself as the agent or mechanism by which the effect is achieved?

For example, we encounter statements such as, ‘global warming will cause the extinction of species such as the polar bear’. The statement is correct, but it identifies only initial cause, leaving ensuing effects unmentioned. The actual process initiated by global warming will result in the melting of the Arctic ice pack. This is the only environment where polar bears can effectively hunt seals, their primary food source (Thomas et al., 2008). Unless the polar bear can adapt behaviorally, and perhaps physiologically, to another major food source, the species will be unable to produce sufficient progeny to avoid continued population decline and extinction. Thus, environmental shift is only the originating cause of background extinction. Such changes in the biological, climatic, or physical environments initiate devolutionary processes that gradually lead to multi-generational background extinction.

Historical examples of background extinction that are even partially documented are rare and invariably include some aspect of human involvement. Nonetheless, the few cases of such extinctions that have been studied in detail typically involve multiple components, e.g. the heath hen (Krebs, 1994). Background extinctions are invariably the result of a series of interacting factors and their multiplicative effects (Gittleman & Gompper, 2001). Likewise, our studies of higher plants show that population decline is related to multiple environmental causes and genetic factors (Wiens et al., 1989, 2002, 2011).

THE MECHANISM OF BACKGROUND EXTINCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. THE ROLE OF EXTINCTION IN BIOHISTORY
  5. THE LINGUISTICS OF EXTINCTION: VOCABULARY, USAGE, SEMANTICS
  6. DEVOLUTION: A WORD TO DESCRIBE THE PROCESS OF BACKGROUND EXTINCTION
  7. BACKGROUND EXTINCTION AS A PROCESS
  8. CLARIFYING THE ISSUE OF EXTINCTION CAUSE
  9. THE MECHANISM OF BACKGROUND EXTINCTION
  10. THE LOSS OF REPRODUCTIVE FITNESS AND EXTINCTION: A THEOREM TOO SIMPLE?
  11. WHY REPRODUCTIVE FITNESS HAS BEEN NEGLECTED AS THE MECHANISM OF BACKGROUND EXTINCTION
  12. CAN THERE BE SELECTION AGAINST REPRODUCTION?
  13. EXTINCTION AMONG SHORT-LIVED SPECIES
  14. LINKING PROXIMATE AND ULTIMATE CAUSES OF BACKGROUND EXTINCTION: REPRODUCTIVE FITNESS AND NORM OF REACTION
  15. NATURAL SELECTION AND BACKGROUND EXTINCTION
  16. THE INCIDENCE OF BACKGROUND EXTINCTION
  17. CLIMATIC SHIFT AND BACKGROUND EXTINCTION
  18. BIOLOGICAL FACTORS AND EXTINCTION
  19. PHASES OF BACKGROUND EXTINCTION: HABITAT ATTENUATION AND DISSOLUTION
  20. CONCLUSIONS
  21. ACKNOWLEDGEMENTS
  22. REFERENCES

‘[scientists] don't write much about background extinctions … because nobody knows how they might occur.’ (Ellis, 2004).

The mechanism of background extinction has remained an enigma for centuries and in recent decades was even imbued with mystical qualities by the use of such descriptive terms as ‘mysterious’ and by questioning whether such a mechanism ‘even exists’. Part of the difficulty may be the absence of a precise definition, as background extinction is often defined by what it is not, i.e. not associated with catastrophic or mass extinctions (Foote & Miller, 2007). It is also referred to as ‘normal, steady, or ongoing’ extinction at relatively low rates. The classic Darwinian view is that background extinction is the result of ongoing evolution in environments with limited resources, where competition is the primary mode of attrition. Although the connection is logical, the competition explanation overlooks the potential complexity of causes and subsequent process. If we consider background extinction as a biological process, a more precise definition is required.

We define background extinction as a typically gradual (but sometimes also surprisingly rapid), multi-generational process of attritional, devolutionary population decline. In this context, rarity is a common antecedent of background extinction, but rarity can also be due to other causes (Rabinowitz, 1981) and is not in itself the cause of extinction (Slobodkin, 1968). However, there is general agreement that rarity increases the probability of extinction from stochastic environmental perturbations as well as genetic factors. We posit that the mechanism of background extinction is the (usually) long-term, multi-generational loss of reproductive (Darwinian) fitness, i.e. the survival value and contribution of a genotype to the next generation.

In cases of suspected population demise, is it more instructive to ask, ‘is there evidence of long-term reproductive failure?’ (a testable hypothesis), as opposed to the more nebulous question, ‘is the population going extinct?’

THE LOSS OF REPRODUCTIVE FITNESS AND EXTINCTION: A THEOREM TOO SIMPLE?

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. THE ROLE OF EXTINCTION IN BIOHISTORY
  5. THE LINGUISTICS OF EXTINCTION: VOCABULARY, USAGE, SEMANTICS
  6. DEVOLUTION: A WORD TO DESCRIBE THE PROCESS OF BACKGROUND EXTINCTION
  7. BACKGROUND EXTINCTION AS A PROCESS
  8. CLARIFYING THE ISSUE OF EXTINCTION CAUSE
  9. THE MECHANISM OF BACKGROUND EXTINCTION
  10. THE LOSS OF REPRODUCTIVE FITNESS AND EXTINCTION: A THEOREM TOO SIMPLE?
  11. WHY REPRODUCTIVE FITNESS HAS BEEN NEGLECTED AS THE MECHANISM OF BACKGROUND EXTINCTION
  12. CAN THERE BE SELECTION AGAINST REPRODUCTION?
  13. EXTINCTION AMONG SHORT-LIVED SPECIES
  14. LINKING PROXIMATE AND ULTIMATE CAUSES OF BACKGROUND EXTINCTION: REPRODUCTIVE FITNESS AND NORM OF REACTION
  15. NATURAL SELECTION AND BACKGROUND EXTINCTION
  16. THE INCIDENCE OF BACKGROUND EXTINCTION
  17. CLIMATIC SHIFT AND BACKGROUND EXTINCTION
  18. BIOLOGICAL FACTORS AND EXTINCTION
  19. PHASES OF BACKGROUND EXTINCTION: HABITAT ATTENUATION AND DISSOLUTION
  20. CONCLUSIONS
  21. ACKNOWLEDGEMENTS
  22. REFERENCES

‘It is time [science] should return to the plainness and soundness of observation on material and obvious things.’ (Hooke, 1665).

The idea that the loss of reproductive fitness is the mechanism of extinction has a long history of dismissal beginning with Wallace's (1858) ternate paper in which he states, ‘The greater or lesser fecundity of an animal is often considered to be one of the chief causes of its abundance or scarcity, but a consideration of the facts will show that it has little or nothing to do with the matter.’

Furthermore, its simplicity in an age of high technology and modelling in the absence of supporting empirical data gives cause for continued neglect or rejection. Yet natural selection itself is a simple idea and is perhaps what prompted T. H. Huxley to comment, ‘How extremely stupid of me not to have thought of that’ (Jones, 2000). Similarly, Morris (2001) points out in relation to the discovery of the polymerase chain reaction (which earned a Nobel Prize) that this was also a simple idea that anyone in the field might have thought of. While Jones (2000) points out that ‘Science can be magnificent in its simplicity’, Young & Clements (2009) also remind us that ‘… science can be exceptionally blind to the obvious’.

Others have suggested that the loss of reproductive fitness (or capacity) was the mechanism of background extinction. Unfortunately, with the exception of Harper (1977), their statements are brief and without elaboration: Jepsen, Mayr & Simpson (1949), Raup (1978, 1984, 1991), McKinney (1993), Rose (1998), Mayr (2001), and no doubt others. Mayr (2001) stated it clearly: ‘Whenever a population is no longer able to reproduce enough offspring to replace losses from natural causes, it will become extinct.’ Perhaps the lack of amplification by these authors was due to the paucity of fecundity data to support the hypothesis (Wiens et al., 2002, 2011; Schoener et al., 2003).

WHY REPRODUCTIVE FITNESS HAS BEEN NEGLECTED AS THE MECHANISM OF BACKGROUND EXTINCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. THE ROLE OF EXTINCTION IN BIOHISTORY
  5. THE LINGUISTICS OF EXTINCTION: VOCABULARY, USAGE, SEMANTICS
  6. DEVOLUTION: A WORD TO DESCRIBE THE PROCESS OF BACKGROUND EXTINCTION
  7. BACKGROUND EXTINCTION AS A PROCESS
  8. CLARIFYING THE ISSUE OF EXTINCTION CAUSE
  9. THE MECHANISM OF BACKGROUND EXTINCTION
  10. THE LOSS OF REPRODUCTIVE FITNESS AND EXTINCTION: A THEOREM TOO SIMPLE?
  11. WHY REPRODUCTIVE FITNESS HAS BEEN NEGLECTED AS THE MECHANISM OF BACKGROUND EXTINCTION
  12. CAN THERE BE SELECTION AGAINST REPRODUCTION?
  13. EXTINCTION AMONG SHORT-LIVED SPECIES
  14. LINKING PROXIMATE AND ULTIMATE CAUSES OF BACKGROUND EXTINCTION: REPRODUCTIVE FITNESS AND NORM OF REACTION
  15. NATURAL SELECTION AND BACKGROUND EXTINCTION
  16. THE INCIDENCE OF BACKGROUND EXTINCTION
  17. CLIMATIC SHIFT AND BACKGROUND EXTINCTION
  18. BIOLOGICAL FACTORS AND EXTINCTION
  19. PHASES OF BACKGROUND EXTINCTION: HABITAT ATTENUATION AND DISSOLUTION
  20. CONCLUSIONS
  21. ACKNOWLEDGEMENTS
  22. REFERENCES

We suggest two primary reasons, in addition to linguistics and the idea that extinction was merely a subset of evolution, as to why the loss of reproductive fitness has not been seriously considered as the mechanism of background extinction. The most critical of these is the widely held perception that the excess generation of progeny also ensures reproductive fitness. Secondly, it is irrational to believe that there can be selection against reproduction (Barish, 2001).

Biologists are well aware of the tenet of excess production of offspring as formulated by Darwin and Wallace in their theory of natural selection, but as Harper (1977) aptly observed, ‘it does not follow that an organism that produces a large number of progeny will also leave a large number of descendants’. Few would deny this statement, but it is foreign to our mind-sets to believe that the generation and/or survival of progeny is insufficient to offset adult mortality and thus initiate population decline. Consequently, the idea is largely ignored, and there is a paucity of long-term demographic studies of populations subjected to changes in the biological or physical environments (Tam in a series of papers, e.g. Tam, 1948, 1972; Oostermeijer, Den Neys & Borgen, 1966; Wiens et al., 2002, 2011; Oostermeijer, Luijten & Den Neys, 2003).

CAN THERE BE SELECTION AGAINST REPRODUCTION?

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. THE ROLE OF EXTINCTION IN BIOHISTORY
  5. THE LINGUISTICS OF EXTINCTION: VOCABULARY, USAGE, SEMANTICS
  6. DEVOLUTION: A WORD TO DESCRIBE THE PROCESS OF BACKGROUND EXTINCTION
  7. BACKGROUND EXTINCTION AS A PROCESS
  8. CLARIFYING THE ISSUE OF EXTINCTION CAUSE
  9. THE MECHANISM OF BACKGROUND EXTINCTION
  10. THE LOSS OF REPRODUCTIVE FITNESS AND EXTINCTION: A THEOREM TOO SIMPLE?
  11. WHY REPRODUCTIVE FITNESS HAS BEEN NEGLECTED AS THE MECHANISM OF BACKGROUND EXTINCTION
  12. CAN THERE BE SELECTION AGAINST REPRODUCTION?
  13. EXTINCTION AMONG SHORT-LIVED SPECIES
  14. LINKING PROXIMATE AND ULTIMATE CAUSES OF BACKGROUND EXTINCTION: REPRODUCTIVE FITNESS AND NORM OF REACTION
  15. NATURAL SELECTION AND BACKGROUND EXTINCTION
  16. THE INCIDENCE OF BACKGROUND EXTINCTION
  17. CLIMATIC SHIFT AND BACKGROUND EXTINCTION
  18. BIOLOGICAL FACTORS AND EXTINCTION
  19. PHASES OF BACKGROUND EXTINCTION: HABITAT ATTENUATION AND DISSOLUTION
  20. CONCLUSIONS
  21. ACKNOWLEDGEMENTS
  22. REFERENCES

The idea that there could be selection against reproduction itself is a more complex issue. It is certainly counter-intuitive. However, extraordinarily high rates of embryonic abortion (95–99%) in several species of flowering plants from the south-western United States may give such an impression (Wiens et al., 1989, 2002, 2011). Similarly high rates of embryonic abortion are also known in some flowering plants from Australia (Meney, Dixon & Pate, 1997; Cochrane et al., 2001) and South Africa (Wiens et al., 1983; Wiens, Davern & Calvin, 1988).

We stress that among these species there is little evidence that the high rates of embryonic abortion rates are strongly influenced by limited resource availability or their re-allocation (Harper & Wallace, 1987; Wiens et al., 1987, 2002, 2011; Marshall & Ludlam, 1989; Owen, 1995; Allphin, Wiens & Harper, 2002; Allphin, Brian & Matheson, 2005, and additional citations listed in those publications). The species in question appear to be long-lived relicts; seedlings are typically rare, but precise, long-term demographic data for seedling survival are available only for Adenostoma sparsifolium Torr. (Rosaceae), a species endemic in the California chaparral (USA) (Wiens et al., 2011).

The levels at which high embryonic abortion rates become critical for population decline (hard selection) are unknown and will probably vary among species. Nevertheless, it is difficult to believe that abortion rates of 95–99% are devolutionarily inconsequential. It also seems counter-intuitive that selection would not reverse such a maladaptive process long before 95–99% of the embryo crop consistently dies. Yet this has not happened.

Six species of flowering plants that have populations with embryonic abortion rates of ∼ 95% occur in arid or semi-arid regions of the Mojave Desert or California chaparral (USA). Three of these species also have exceptionally high rates of genetic variation in comparison with other seed plants with similar growth forms, breeding systems, and longevity (Nickrent & Wiens, 1989; Wiens et al., 1989, 2011; Hamrick & Godt, 1990). Genetic variation in the other three species remains to be studied. But why should there be a relationship between high levels of heterozygosity and excessive rates of embryonic abortion, particularly when heterozygosity is considered a critical factor in population viability and adaptability?

We postulate that the high rates of heterozygosity observed in these species is a strategy for survival under conditions of increasing aridity (Nickrent & Wiens, 1989; Wiens et al., 1989, 2011) that has affected the region since approximately the mid-Holocene (Axelrod, 1989). Heterosis is well known to impart physiological advantages in stressful environments (Mitton, 1993) and levels of heterozygosity are responsive to selection (Mitton et al., 1993). A large body of data shows that heterozygosity is usually beneficial because it produces adaptive advantages from heterosis (Schaal & Levin, 1976).

However, promoting survival by raising the levels of heterozygous overdominance (balanced or segregational genetic load) also carries with it the potential for increasing the number of recessive deleterious and lethal developmental alleles. When such alleles recombine as homozygotes at fertilization they are initially exposed to selection during embryonic differentiation when developmental genes are first activated by the zygotic genome (Hedrick, 2005). This results in embryonic abortion, but progeny death can also occur at later developmental stages, e.g. sickle cell anaemia. Only several unlinked lethals are necessary to produce high percentages of aborted embryos (Allendorf & Luikart, 2007). Such deleterious or lethal developmental alleles are well known in plants and animals (see Wiens et al., 2011 for plant examples).

In addition, most of the plant species with high rates of embryonic abortion are long-lived and age is correlated with increased mutational load that could further contribute to embryonic abortion (Klekowski, 1988). Moreover, as population size is reduced, other detrimental genetic factors may come into play, e.g. genetic drift (Rice, 2004), and as previously mentioned, it is also generally recognized that small populations are more susceptible to extinction from stochastic environmental events (Gilpin & Soulé, 1986).

But why should selection for heterozygosity be so strong that the trend would not be reversed prior to reaching these exceptional levels of embryonic death? We posit that these highly elevated abortion rates do not, in fact, represent selection against reproduction per se. Rather, we stress that they are inadvertent artefacts of the exceptionally high rates of heterozygous overdominance necessary for survival. Because selection is not prescient, increasing levels of heterozygosity would continue (in spite of increasing rates of embryonic abortion) because individual survival will always, perforce, take precedence over any other aspect of fitness, including reproduction. As a corollary, the trend is not reversed because progeny with lower levels of heterozygosity would probably not survive. This apparent paradox might be considered a ‘devolutionary catch-22’, i.e. if individuals are able to survive, they might not be able to reproduce, but if their reproductive potential is increased, they might not survive!

Many of our examples are drawn from higher plants, but we emphasize that the phenomena they illustrate are also often applicable to higher animals, and are not necessarily peculiar attributes of plants. Higher plants possess many advantages in studies of reproduction and extinction that are not fully appreciated (Harper & Wallace, 1987). Furthermore, the mechanism we propose does not exclude short-lived species, as extinction will still be multi-generational, even though relatively few generations are required. Furthermore, the ‘catch-22’ described above may still operate, with selection favouring heterozygosity as expressed in a stage other than adulthood, e.g. prolonged dormancy of seeds in plants or of pupae or larvae in invertebrates.

EXTINCTION AMONG SHORT-LIVED SPECIES

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. THE ROLE OF EXTINCTION IN BIOHISTORY
  5. THE LINGUISTICS OF EXTINCTION: VOCABULARY, USAGE, SEMANTICS
  6. DEVOLUTION: A WORD TO DESCRIBE THE PROCESS OF BACKGROUND EXTINCTION
  7. BACKGROUND EXTINCTION AS A PROCESS
  8. CLARIFYING THE ISSUE OF EXTINCTION CAUSE
  9. THE MECHANISM OF BACKGROUND EXTINCTION
  10. THE LOSS OF REPRODUCTIVE FITNESS AND EXTINCTION: A THEOREM TOO SIMPLE?
  11. WHY REPRODUCTIVE FITNESS HAS BEEN NEGLECTED AS THE MECHANISM OF BACKGROUND EXTINCTION
  12. CAN THERE BE SELECTION AGAINST REPRODUCTION?
  13. EXTINCTION AMONG SHORT-LIVED SPECIES
  14. LINKING PROXIMATE AND ULTIMATE CAUSES OF BACKGROUND EXTINCTION: REPRODUCTIVE FITNESS AND NORM OF REACTION
  15. NATURAL SELECTION AND BACKGROUND EXTINCTION
  16. THE INCIDENCE OF BACKGROUND EXTINCTION
  17. CLIMATIC SHIFT AND BACKGROUND EXTINCTION
  18. BIOLOGICAL FACTORS AND EXTINCTION
  19. PHASES OF BACKGROUND EXTINCTION: HABITAT ATTENUATION AND DISSOLUTION
  20. CONCLUSIONS
  21. ACKNOWLEDGEMENTS
  22. REFERENCES

Short-lived organisms with rapid generation times do not have the option of postponing reproduction as do long-lived organisms. To largely miss a reproductive season could result in a serious population crash, particularly among small mammals. Thus, it is not surprising that such species have evolved enormous reproductive capacities. However, the frequent generation of high rates of viable progeny is generally associated with low genetic variability that carries with it other extinction risks.

We posit that populations of short-lived species with characteristically low genetic variability and rapid generation times are more susceptible to rapid extinction from extreme environmental perturbations because they do not possess the genetic variability to adapt to rapid biological or climatic shifts and severe environmental changes could also disrupt the rapid generation cycle. Thus, population extinction may occur with exceptional rapidity among such organisms, but will nonetheless generally occur over at least a few generations.

Most of the discussion relating to background extinction to this point has centred on long-lived, woody plants adapted for cross-pollination that are genetically heterozygous (Hamrick & Godt, 1990). Such plants average seed-sets of only ∼ 30% due to high rates of embryonic abortion (Wiens, 1984; Wiens et al., 1987). In contrast, annual or short-lived herbaceous species are generally self-pollinated and the populations are genetically homozygous. Such species successfully mature ∼ 90% or more of both fruits and seeds (Wiens, 1984; Harper & Wallace, 1987; Wiens et al., 1987).

Perpetually self-pollinating plants do not retain recessive lethal or deleterious alleles, because any such mutations are rapidly exposed to selection and removed from the population. In effect, self-pollinated short-lived plants are essentially ‘reproductive machines’. Not surprisingly they are also among our most pernicious weeds. [Somehow poets always seem to capture the essence of a situation better than expository prose, e.g. ‘… weeds come on and on in irrepressible regiments’ (Sandberg, 1920).]

The relationships between longevity, genetic heterozygosity, and reproductive capacity noted in flowering plants are also paralleled in higher animals. All higher animals have separate sexes and obviously cross breed. African elephants have a lifespan of ∼ 50 years and exhibit high levels of both observed and expected heterozygosity (He, 0.68) (Nyakaana, Arctander & Siegismund, 2002). Females reach sexual maturity in ∼ 15 years and produce one offspring every 5 years for roughly 30 years, but juvenile mortality is high (61%) (Moss, 2001).

Small mammals can be compared with short-lived, genetically homozygous plant species with high reproductive output, whose lifespans do not generally exceed a year. Voles provide a good example. They reach sexual maturity in about a month and can produce five or more litters of 5–10 young during a season, thus generating potentially massive population increases in a relatively short time (Whitaker & Hamilton, 1998). In Microtus subterraneous, genetic diversity is predictably low (He, 0.043) with high fixation indices (0.528) that suggest overall heterozygote deficiencies (Macholan, Filippuccii & Zima, 2001). Needless to say some small animals can also be considered ‘weedy reproductive machines’.

Spontaneous embryonic abortion is difficult to measure in mammals, as opposed the higher plants (Harper & Wallace, 1987; Wiens et al., 1987). Long-lived, heterozygous flowering plants have an overall embryonic abortion rate of ∼ 50% (Wiens, 1984). Extensive data on spontaneous embryonic abortions in higher animals are available only for humans, which also average ∼ 50–60% (Smith, 2008). Attributing spontaneous embryonic abortion rates in both higher plants and animals to the same cause, i.e. high levels of heterozygosity, might seem questionable. But consider that both groups are eukaryotes, have virtually identical genetic systems, as well as the same mode of gene action.

In many ways small mammals might be more vulnerable to short-term extinction than short-lived plants because annual and short-lived perennials are able to survive decades of adverse environments as seeds. For example, the seed banks of many desert annuals are well known to remain dormant for decades before a favourable environmental event stimulates germination. Although small mammals can survive adverse seasonal environments by hibernation, we are unaware that they can hibernate for more than a single season. Thus, small mammals have no apparent multiple-year escapes from shifting environments, except emigration to more favourable habitats, if available. Such an emigration has occurred among small mammals in Yosemite National Park, California, where small mammals have expanded their distributions by migrating to higher elevations as climate has warmed (Craig et al., 2008).

In contrast, the pika, a small mammal endemic in the alpine ecosystems of the western USA, has no such migratory options. Commensurate with climatic warming various populations of pikas have disappeared from a number of alpine habitats over the last several decades (Patterson, 1984; Beever, Brussard & Berger, 2003). An additional example is discussed under Habitat Dissolution.

Thus, short-lived species sacrifice genetic variability for short-term reproductive success, but as a consequence are subject to rapid extinction if environments change. In contrast, long-lived heterozygous organisms, because of their heterotic advantages, are not only able to survive relatively short-term environmental extremes, but can often persist for relatively long periods following environmental shifts while their populations slowly decline and ultimately succumb to background extinction.

LINKING PROXIMATE AND ULTIMATE CAUSES OF BACKGROUND EXTINCTION: REPRODUCTIVE FITNESS AND NORM OF REACTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. THE ROLE OF EXTINCTION IN BIOHISTORY
  5. THE LINGUISTICS OF EXTINCTION: VOCABULARY, USAGE, SEMANTICS
  6. DEVOLUTION: A WORD TO DESCRIBE THE PROCESS OF BACKGROUND EXTINCTION
  7. BACKGROUND EXTINCTION AS A PROCESS
  8. CLARIFYING THE ISSUE OF EXTINCTION CAUSE
  9. THE MECHANISM OF BACKGROUND EXTINCTION
  10. THE LOSS OF REPRODUCTIVE FITNESS AND EXTINCTION: A THEOREM TOO SIMPLE?
  11. WHY REPRODUCTIVE FITNESS HAS BEEN NEGLECTED AS THE MECHANISM OF BACKGROUND EXTINCTION
  12. CAN THERE BE SELECTION AGAINST REPRODUCTION?
  13. EXTINCTION AMONG SHORT-LIVED SPECIES
  14. LINKING PROXIMATE AND ULTIMATE CAUSES OF BACKGROUND EXTINCTION: REPRODUCTIVE FITNESS AND NORM OF REACTION
  15. NATURAL SELECTION AND BACKGROUND EXTINCTION
  16. THE INCIDENCE OF BACKGROUND EXTINCTION
  17. CLIMATIC SHIFT AND BACKGROUND EXTINCTION
  18. BIOLOGICAL FACTORS AND EXTINCTION
  19. PHASES OF BACKGROUND EXTINCTION: HABITAT ATTENUATION AND DISSOLUTION
  20. CONCLUSIONS
  21. ACKNOWLEDGEMENTS
  22. REFERENCES

Reproductive fitness will be reduced in successive generations when the extremes of an environmental shift frequently exceed the norms of reaction (range of phenotypic responses of a genotype to different environments) to which the species is adapted (Schlichting & Massimo, 1998). This is the most vital of issues because adaptations to environmental shifts (especially climatic) often occur as changes in the physio-biochemical functions that comprise the norm of reaction. These processes will be most evident at the margins of distribution and can adversely affect reproduction following unfavourable environmental perturbations (Pigott & Huntley, 1981; Dorken & Eckert, 2001; Jump & Woodward, 2003). If environmental extremes approach lethal thresholds over multiple generations, and the norm of reaction is unable to adapt, reproductive fitness will necessarily be sacrificed in favour of selection for individual survival. Population decline will inevitably follow, as demonstrated in tropical lizards (Sinervo et al., 2010).

Likewise, the first response of higher plants subjected to water stress, or other resource limitations, will be to reduce or even eliminate reproductive growth (Harper, 1977). Similarly, animals forego reproduction in resource-limited seasons. As Schlichting & Massimo (1998) comment, organisms whose norms of reaction are unable to respond appropriately to continued environmental extremes (or emigrate) are ‘long since extinct’. Establishing norm of reaction responses for species subjected to shifting environments is an important area for physiological ecology (Clausen, Keck & Hiesey, 1940; Billings, 1957; Bazzaz, 1996). However, results are rarely related to long-term studies of change in population size (e.g. Pauli, Gottfried & Grabherr, 1999; Jepsen et al., 2008).

NATURAL SELECTION AND BACKGROUND EXTINCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. THE ROLE OF EXTINCTION IN BIOHISTORY
  5. THE LINGUISTICS OF EXTINCTION: VOCABULARY, USAGE, SEMANTICS
  6. DEVOLUTION: A WORD TO DESCRIBE THE PROCESS OF BACKGROUND EXTINCTION
  7. BACKGROUND EXTINCTION AS A PROCESS
  8. CLARIFYING THE ISSUE OF EXTINCTION CAUSE
  9. THE MECHANISM OF BACKGROUND EXTINCTION
  10. THE LOSS OF REPRODUCTIVE FITNESS AND EXTINCTION: A THEOREM TOO SIMPLE?
  11. WHY REPRODUCTIVE FITNESS HAS BEEN NEGLECTED AS THE MECHANISM OF BACKGROUND EXTINCTION
  12. CAN THERE BE SELECTION AGAINST REPRODUCTION?
  13. EXTINCTION AMONG SHORT-LIVED SPECIES
  14. LINKING PROXIMATE AND ULTIMATE CAUSES OF BACKGROUND EXTINCTION: REPRODUCTIVE FITNESS AND NORM OF REACTION
  15. NATURAL SELECTION AND BACKGROUND EXTINCTION
  16. THE INCIDENCE OF BACKGROUND EXTINCTION
  17. CLIMATIC SHIFT AND BACKGROUND EXTINCTION
  18. BIOLOGICAL FACTORS AND EXTINCTION
  19. PHASES OF BACKGROUND EXTINCTION: HABITAT ATTENUATION AND DISSOLUTION
  20. CONCLUSIONS
  21. ACKNOWLEDGEMENTS
  22. REFERENCES

We are accustomed to thinking of selection as a positive force leading to increased reproductive fitness that is universally recognized as the mechanism of adaptation and speciation. But selection has a broader role in biology and both evolution and devolution can be thought of as the products of either positive or negative selection (Raup, 1984; Grant, 1991). Evolution and devolution are merely subordinate categories of the more encompassing science of natural selection that is also applicable to other fields, e.g. economics (Omerod, 2005). Natural selection is therefore the mechanism by which the shifting forces of the biological and/or physical environments have determined the survival, evolution, or extinction of species through biohistory. Darwin was clearly aware of the central role of natural selection in extinction: ‘… extinction accords well with the theory of natural selection’. But we are unaware that he ever expanded the idea and also suspect that he was thinking largely in terms of competition.

THE INCIDENCE OF BACKGROUND EXTINCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. THE ROLE OF EXTINCTION IN BIOHISTORY
  5. THE LINGUISTICS OF EXTINCTION: VOCABULARY, USAGE, SEMANTICS
  6. DEVOLUTION: A WORD TO DESCRIBE THE PROCESS OF BACKGROUND EXTINCTION
  7. BACKGROUND EXTINCTION AS A PROCESS
  8. CLARIFYING THE ISSUE OF EXTINCTION CAUSE
  9. THE MECHANISM OF BACKGROUND EXTINCTION
  10. THE LOSS OF REPRODUCTIVE FITNESS AND EXTINCTION: A THEOREM TOO SIMPLE?
  11. WHY REPRODUCTIVE FITNESS HAS BEEN NEGLECTED AS THE MECHANISM OF BACKGROUND EXTINCTION
  12. CAN THERE BE SELECTION AGAINST REPRODUCTION?
  13. EXTINCTION AMONG SHORT-LIVED SPECIES
  14. LINKING PROXIMATE AND ULTIMATE CAUSES OF BACKGROUND EXTINCTION: REPRODUCTIVE FITNESS AND NORM OF REACTION
  15. NATURAL SELECTION AND BACKGROUND EXTINCTION
  16. THE INCIDENCE OF BACKGROUND EXTINCTION
  17. CLIMATIC SHIFT AND BACKGROUND EXTINCTION
  18. BIOLOGICAL FACTORS AND EXTINCTION
  19. PHASES OF BACKGROUND EXTINCTION: HABITAT ATTENUATION AND DISSOLUTION
  20. CONCLUSIONS
  21. ACKNOWLEDGEMENTS
  22. REFERENCES

The loss of reproductive fitness as the mechanism of background extinction does not (as might be supposed) contradict Darwin and Wallace's tenet that excess production of progeny is a major feature of evolutionary theory. This is because > 99% of all species in relatively stable ecosystems do, in fact, generate excess progeny of which sufficient numbers survive to maintain or expand population numbers. But it is precisely the < 1% of species in such ecosystems that are apt to be in the process of background extinction at any one time. This is largely a continuous, ongoing process in most biotic communities, where there are typically a few species that are expanding (evolving) and a few that are in decline (devolving). In many such cases, the devolving populations are, or will become, relicts.

As an example, there are five species of flowering plants in the northern Mojave Desert of California, from a total number 1237 species listed by DeDecker (1984), that have exceedingly limited, if any, reproductive potential (Wiens et al., 1989, 2002). Of these five species, at least four can be considered relicts. In addition, three species from the California chaparral exhibit similar loss of reproductive capacity (Wiens et al., 2011).

There is irony in the fact that such a small proportion of species (∼ 1%) appear to be in the process of devolutionary decline at any particular time, when through the course of biohistory < 95% of all species have gone extinct due to background extinction (Raup, 1994).

CLIMATIC SHIFT AND BACKGROUND EXTINCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. THE ROLE OF EXTINCTION IN BIOHISTORY
  5. THE LINGUISTICS OF EXTINCTION: VOCABULARY, USAGE, SEMANTICS
  6. DEVOLUTION: A WORD TO DESCRIBE THE PROCESS OF BACKGROUND EXTINCTION
  7. BACKGROUND EXTINCTION AS A PROCESS
  8. CLARIFYING THE ISSUE OF EXTINCTION CAUSE
  9. THE MECHANISM OF BACKGROUND EXTINCTION
  10. THE LOSS OF REPRODUCTIVE FITNESS AND EXTINCTION: A THEOREM TOO SIMPLE?
  11. WHY REPRODUCTIVE FITNESS HAS BEEN NEGLECTED AS THE MECHANISM OF BACKGROUND EXTINCTION
  12. CAN THERE BE SELECTION AGAINST REPRODUCTION?
  13. EXTINCTION AMONG SHORT-LIVED SPECIES
  14. LINKING PROXIMATE AND ULTIMATE CAUSES OF BACKGROUND EXTINCTION: REPRODUCTIVE FITNESS AND NORM OF REACTION
  15. NATURAL SELECTION AND BACKGROUND EXTINCTION
  16. THE INCIDENCE OF BACKGROUND EXTINCTION
  17. CLIMATIC SHIFT AND BACKGROUND EXTINCTION
  18. BIOLOGICAL FACTORS AND EXTINCTION
  19. PHASES OF BACKGROUND EXTINCTION: HABITAT ATTENUATION AND DISSOLUTION
  20. CONCLUSIONS
  21. ACKNOWLEDGEMENTS
  22. REFERENCES

In a 15-year empirical study of population demographics in Adenostoma sparsifolium, a rosaceous shrub endemic in the California chaparral, there is clear evidence of attritional, devolutionary population decline (Wiens et al., 2011). This loss is attributable to a climatic shift toward increasing aridity (particularly the loss of summer rain) during the mid-Holocene thermal optimum (hypsithermal) (Axelrod, 1989). This species is characterized by either the virtual absence of seedlings following wildfires, or the inability of occasional seedlings to survive the extended summer drought typical of the present chaparral climate. In the geological short-term (hundreds, thousands? of years) A. sparsifolium survives only because its large lignotubers possess great longevity and readily sprout shoots following the frequent (∼ 20 years) occurrence of wildfires in chaparral (Radtke, Arndt & Wakimoto, 1982).

However, without new reproduction and a low but continuous ∼ 6% rate of adult mortality following wildfire, extinction is inevitable. Additional mortality from prolonged (5-year) drought and stochastic environmental disturbances will accelerate the process. Furthermore, this species also has populations with astonishingly high levels of allozyme variability and genetically mediated embryonic abortion (95–99%), thus reducing seed-set to only 1–5% of the original embryo crop (Wiens et al., 2011). The increased frequency of wildfires that presumably accompanied the Holocene hypsithermal, greatly complemented by current anthropogenic causes of wildfire (Pinter, Fiedel & Keeley, 2011), have therefore acted as a secondary devolutionary agent, stemming from an original climatic shift toward greater aridity. Thus, in A. sparsifolium, we see a clear distinction between proximate and ultimate causes of population decline.

BIOLOGICAL FACTORS AND EXTINCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. THE ROLE OF EXTINCTION IN BIOHISTORY
  5. THE LINGUISTICS OF EXTINCTION: VOCABULARY, USAGE, SEMANTICS
  6. DEVOLUTION: A WORD TO DESCRIBE THE PROCESS OF BACKGROUND EXTINCTION
  7. BACKGROUND EXTINCTION AS A PROCESS
  8. CLARIFYING THE ISSUE OF EXTINCTION CAUSE
  9. THE MECHANISM OF BACKGROUND EXTINCTION
  10. THE LOSS OF REPRODUCTIVE FITNESS AND EXTINCTION: A THEOREM TOO SIMPLE?
  11. WHY REPRODUCTIVE FITNESS HAS BEEN NEGLECTED AS THE MECHANISM OF BACKGROUND EXTINCTION
  12. CAN THERE BE SELECTION AGAINST REPRODUCTION?
  13. EXTINCTION AMONG SHORT-LIVED SPECIES
  14. LINKING PROXIMATE AND ULTIMATE CAUSES OF BACKGROUND EXTINCTION: REPRODUCTIVE FITNESS AND NORM OF REACTION
  15. NATURAL SELECTION AND BACKGROUND EXTINCTION
  16. THE INCIDENCE OF BACKGROUND EXTINCTION
  17. CLIMATIC SHIFT AND BACKGROUND EXTINCTION
  18. BIOLOGICAL FACTORS AND EXTINCTION
  19. PHASES OF BACKGROUND EXTINCTION: HABITAT ATTENUATION AND DISSOLUTION
  20. CONCLUSIONS
  21. ACKNOWLEDGEMENTS
  22. REFERENCES

Discussion to this point has centred largely on climatic shifts in relation to background extinction. However, biological factors are also important. Typically these include coextinction, competition, disease, and predation. There is an immense literature on these subjects and we will only present a brief synopsis. With the exception of coextinction and predation, these appear to be of less importance in devolutionary decline and background extinction than climatic change.

Coextinction will probably become a critical factor in extinction as members of co-evolved systems (e.g. plant/pollinator relationships) are extirpated. Thus, coextinction, unlike the other factors, has the potential for initiating a cascading series of extinction events.

Competition is perhaps more important among animals than plants, and the result is more often avoidance rather than the extinction of one of the competing species.

Disease and pandemics can result in dramatic population crashes, e.g. bubonic plague and influenza among humans, but we are unaware of species extinctions resulting from disease. Inevitably, there are some resistant survivors in most populations.

The introduction of alien predators is the most important single biological cause of extinction and a number of such extinctions are now well documented. The changes necessary for adaptation by prey species to coexist with recently introduced predators are far greater than is possible over the time periods available.

The most important aspect of biological causes in terms of extinction is perhaps their interaction with other changes in the environment that produce the multiplicity of factors that typically result in extinction.

PHASES OF BACKGROUND EXTINCTION: HABITAT ATTENUATION AND DISSOLUTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. THE ROLE OF EXTINCTION IN BIOHISTORY
  5. THE LINGUISTICS OF EXTINCTION: VOCABULARY, USAGE, SEMANTICS
  6. DEVOLUTION: A WORD TO DESCRIBE THE PROCESS OF BACKGROUND EXTINCTION
  7. BACKGROUND EXTINCTION AS A PROCESS
  8. CLARIFYING THE ISSUE OF EXTINCTION CAUSE
  9. THE MECHANISM OF BACKGROUND EXTINCTION
  10. THE LOSS OF REPRODUCTIVE FITNESS AND EXTINCTION: A THEOREM TOO SIMPLE?
  11. WHY REPRODUCTIVE FITNESS HAS BEEN NEGLECTED AS THE MECHANISM OF BACKGROUND EXTINCTION
  12. CAN THERE BE SELECTION AGAINST REPRODUCTION?
  13. EXTINCTION AMONG SHORT-LIVED SPECIES
  14. LINKING PROXIMATE AND ULTIMATE CAUSES OF BACKGROUND EXTINCTION: REPRODUCTIVE FITNESS AND NORM OF REACTION
  15. NATURAL SELECTION AND BACKGROUND EXTINCTION
  16. THE INCIDENCE OF BACKGROUND EXTINCTION
  17. CLIMATIC SHIFT AND BACKGROUND EXTINCTION
  18. BIOLOGICAL FACTORS AND EXTINCTION
  19. PHASES OF BACKGROUND EXTINCTION: HABITAT ATTENUATION AND DISSOLUTION
  20. CONCLUSIONS
  21. ACKNOWLEDGEMENTS
  22. REFERENCES

Background extinction is divisible into two intergrading stages: habitat attenuation and habitat dissolution. Both categories bear resemblances to extinction patterns known as ecological traps and blind alleys (Simpson, 1953), to some aspects of taxon cycles (Wilson, 1961), and to extinction vortex models (Gilpin & Soulé, 1986). However, patterns do not necessarily explain the mechanism responsible for background extinctions.

Habitat attenuation

This is the persistent loss of survivable habitat and/or niche in response to various shifts in the biological, climatic, or physical environments. Such shifts can result in the reduction and fragmentation of species into a series of smaller, often relict, populations (Oostermeijer et al., 2003; Hampe & Petit, 2005; Dobrowski, 2011; Hampe & Jump, 2011). The overall environment in these relict populations will probably remain amenable for adult survival, and reproductive output is not necessarily compromised. However, progeny survival is doubtful because of continuing loss of habitat/niche. Thus, the effect is nonetheless manifest as the loss of reproductive fitness through devolutionary decline because replacement will not continue to equal adult mortality, even though there is an excess generation of progeny.

There are many instances, worldwide, of individual species or suites of species that survive in what are essentially relict habitats. For example, Eucalyptus caesia (Myrtaceae) is restricted to granite outcrops in western Australia (Byrne & Hopper, 2008), and many isolated stands of Pacific coast forest in Montana and Idaho (USA) are far removed from the primary distribution of this major forest ecosystem west of the Cascade Mountains (Benson, 1979).

The geographical distributions of species are essentially defined by the limits of their norms of reaction. As previously discussed, norms of reaction involve numerous integrated physiological processes. When environments change, particularly climate, it is typically the marginal populations that are initially affected, as they already function at the limits of their reaction norms (Pigott & Huntley, 1981). If the shift continues and emigration to suitable habitat is impossible, habitat attenuation will continue until populations are restricted to only the most favourable sites.

We suspect that many environmental shifts occur either too rapidly for organisms to adapt their norms of reaction to the changing conditions (e.g. current global warming), or the shift is of such magnitude that adaptation is impossible (e.g. the introduction of aggressive alien predators). The process of habitat attenuation is substantiated by numerous, worldwide examples of populations, or small suites of species, that now occur in restricted habitats surrounded by species characteristic of wholly different ecosystems (Dobrowski, 2011). A number of relict plant species occur in the California flora that have fossil records indicating much larger distributions in the geological past (Ornduff, Faber & Keeler-Wolf, 2003). One of the best known examples is the giant sequoia [Sequoiadendron gigantea (Lindley) Buchholz], which had a much broader distribution in the Miocene (Hartesveldt et al., 1981).

Animal examples of habitat attenuation show how quickly these changes can occur. Anthropogenic global warming began about 150 years ago with the end of the Little Ice Age (IPCC, 2007). Yet by 1984 it was observed that the habitat of the pika, a small mammal occurring in the alpine regions of the western United States, was gradually attenuating as a result of global warming (Patterson, 1984; Beever et al., 2003). Likewise, the habitat of the California alpine chipmonk (Tamias alpinus) is also in decline (Craig et al., 2008). Species occupying extreme environments, e.g. alpine tundra, are perhaps more susceptible to climatic shifts because they have limited, if any, emigration potential (Grabherr, Gottfried & Pauli, 1994). The impending extinction crisis is largely the result of human-mediated habitat attenuation, and to a lesser extent hunting overkill, disease, introduction of alien species, and coextinction, in which species become extinct as a result of loss of another species upon which it depends (Diamond, 1984, 1989).

Habitat dissolution

This is the culmination of habitat attenuation and is the final stage of background extinction. The original environment to which the species was adapted is now greatly altered or may even have disappeared. Adult individuals may persist, albeit at the margin of their norms of reaction. However, a devolutionary threshold has been crossed, after which self-perpetuating effects set the species on a path of irrevocable devolutionary decline and extinction (Shaffer, 1981; Wiens et al., 2011). In effect, a new community of organisms has organized around the surviving relict populations (Hampe & Jump, 2011). Such species are ecodisplaced, i.e. they are ecologically ‘out of place’ because they possess few physiological, morphological, or genetic characteristics that adapt them for long-term survival and effective reproduction in the transformed environment in which they now occur (Wiens et al., 1989, 2002, 2011; Jones, Mace & Purvis, 2000).

Populations of long-lived species suspected of being ecodisplaced might be identified by a population structure that is heavily skewed toward old individuals, as in populations of Juniperus deppeana Steud. (Cupressaceae) in the south-western United States (Patterson, 1984), or the virtual absence of seedlings or juveniles in several Californian endemic plants, namely Adenostoma sparsifolium (Rosaceae) (Wiens et al., 2011), Dedeckera (Polygonaceae) (Wiens et al., 1989), and Xylococcus (Ericaceae) (Keeley & Davis, 2007).

Another example of climate change initiating biological effects that lead to population decline is found in tropical lizards. In this case, increasingly high ambient temperatures have exceeded the norm of reaction that allows lizards to reproduce normally (Sinervo et al., 2010). Lizards must bask in the sun to raise body temperatures sufficiently to hunt effectively. However, lizards must seek shade before physiological high temperature limits are exceeded. The increasing temperatures of tropical habitats now preclude adequate hunt-time before lizards must find shade. Thus, females are unable to acquire the nutritional levels necessary for successful embryonic development, thereby initiating population decline.

This example suggests that in cases of greatly accelerated environmental shifts, yet still requiring multiple generations, habitat attenuation is essentially circumvented and such populations can move directly into habitat dissolution. Such rapid devolutionary declines that result in extinction appear to be common, particularly among short-lived organisms. Because of the comparative frequency of such extinctions it might be useful to identify them as ‘quasi-catastrophic’.

CONCLUSIONS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. THE ROLE OF EXTINCTION IN BIOHISTORY
  5. THE LINGUISTICS OF EXTINCTION: VOCABULARY, USAGE, SEMANTICS
  6. DEVOLUTION: A WORD TO DESCRIBE THE PROCESS OF BACKGROUND EXTINCTION
  7. BACKGROUND EXTINCTION AS A PROCESS
  8. CLARIFYING THE ISSUE OF EXTINCTION CAUSE
  9. THE MECHANISM OF BACKGROUND EXTINCTION
  10. THE LOSS OF REPRODUCTIVE FITNESS AND EXTINCTION: A THEOREM TOO SIMPLE?
  11. WHY REPRODUCTIVE FITNESS HAS BEEN NEGLECTED AS THE MECHANISM OF BACKGROUND EXTINCTION
  12. CAN THERE BE SELECTION AGAINST REPRODUCTION?
  13. EXTINCTION AMONG SHORT-LIVED SPECIES
  14. LINKING PROXIMATE AND ULTIMATE CAUSES OF BACKGROUND EXTINCTION: REPRODUCTIVE FITNESS AND NORM OF REACTION
  15. NATURAL SELECTION AND BACKGROUND EXTINCTION
  16. THE INCIDENCE OF BACKGROUND EXTINCTION
  17. CLIMATIC SHIFT AND BACKGROUND EXTINCTION
  18. BIOLOGICAL FACTORS AND EXTINCTION
  19. PHASES OF BACKGROUND EXTINCTION: HABITAT ATTENUATION AND DISSOLUTION
  20. CONCLUSIONS
  21. ACKNOWLEDGEMENTS
  22. REFERENCES

We posit that the mechanism of background extinction is a typically long-term, multi-generational loss of reproductive fitness that is generally the result of both environmental and genetic factors. A lack of adequate vocabulary is largely responsible for our failure to recognize that the mechanism of background extinction is the loss of reproductive fitness and that it is a process that requires time and produces an effect. The absence of such terminology resulted in attributing extinction largely to cause(s) and in so doing seemingly expanding the concept of ‘cause’ to be inclusive of effect. To provide a terminology to express background extinction as a process, we propose the term devolution. Thus, evolution is a positive force leading to adaptation and speciation, while devolution is a negative process resulting in population decline and background extinction. Both are the products of natural selection.

Only a small proportion of species are apt to be in the process of background extinction at any particular time, although the process will be faster during massive extinction events. Nonetheless background extinction is responsible for the vast majority of all extinctions through biohistory.

Under conditions of continuing adverse climatic change among long-lived species, selection will shift from maintaining populational reproductive fitness to individual survival. At least among higher plants the shift to individual survival was accomplished by selecting for heterozygous overdominance. However, this had the unfortunate side effect of increasing the number of deleterious and lethal alleles expressed during embryogenesis, thereby decreasing fecundity, sometimes dramatically.

Short-lived organisms, such as annual plants and small mammals (occasionally long-lived organisms), generally maintain low levels of genetic variation and have high reproductive capacities. Such species can be swift colonizers and are prone to ‘weedyness’ when habitats are disturbed. However, because of their low genetic variability such organisms have reduced adaptive potential during severe environmental shifts and are thus subject to rapid (quasi-catastrophic?) extinction. In contrast, long-lived organisms tend to devolve and slowly succumb to background extinction.

Background extinction is divided into two intergrading phases of a continuum: habitat attenuation is the process that precludes survival of progeny because of continued loss of suitable habitat/niche. Habitat dissolution is the final stage of background extinction. The habitat to which the species is adapted has now essentially disappeared and it has few, if any, adaptations that permit successful reproduction in the transformed environment.

REFERENCES

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. THE ROLE OF EXTINCTION IN BIOHISTORY
  5. THE LINGUISTICS OF EXTINCTION: VOCABULARY, USAGE, SEMANTICS
  6. DEVOLUTION: A WORD TO DESCRIBE THE PROCESS OF BACKGROUND EXTINCTION
  7. BACKGROUND EXTINCTION AS A PROCESS
  8. CLARIFYING THE ISSUE OF EXTINCTION CAUSE
  9. THE MECHANISM OF BACKGROUND EXTINCTION
  10. THE LOSS OF REPRODUCTIVE FITNESS AND EXTINCTION: A THEOREM TOO SIMPLE?
  11. WHY REPRODUCTIVE FITNESS HAS BEEN NEGLECTED AS THE MECHANISM OF BACKGROUND EXTINCTION
  12. CAN THERE BE SELECTION AGAINST REPRODUCTION?
  13. EXTINCTION AMONG SHORT-LIVED SPECIES
  14. LINKING PROXIMATE AND ULTIMATE CAUSES OF BACKGROUND EXTINCTION: REPRODUCTIVE FITNESS AND NORM OF REACTION
  15. NATURAL SELECTION AND BACKGROUND EXTINCTION
  16. THE INCIDENCE OF BACKGROUND EXTINCTION
  17. CLIMATIC SHIFT AND BACKGROUND EXTINCTION
  18. BIOLOGICAL FACTORS AND EXTINCTION
  19. PHASES OF BACKGROUND EXTINCTION: HABITAT ATTENUATION AND DISSOLUTION
  20. CONCLUSIONS
  21. ACKNOWLEDGEMENTS
  22. REFERENCES
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