Mammalian Evolution, Diversity and Systematics

Frank Zachos, Robert Asher

• Publisher: De Gruyter
• Year: 2018
• ISBN:
  9783110382549
• Edition: 1
• Topic: Biological Sciences
• Subtopic: Entomology
• Index: Biological Sciences

There are nearly 6, 000 mammalian species, among them our own. Research on our evolutionary cousins has a long history, but the last 20 years have seen particularly rapid progress in disentangling the interrelationships and evolutionary history of mammals. The present volume combines up-to-date reviews on mammalian phylogenetics with paleontological, taxonomic and evolutionary chapters and also summarizes the historical development of our insights in mammalian relationships, and thus our own place in the Tree of Life. Our book places the present biodiversity crisis in context, with one in four mammal species threatened by extinction, and reviews the distribution and conservation of mammalian diversity across the globe. This volume is the introductory tome to the new Mammalia series of the Handbook of Zoology and will be essential reading for mammalogists, zoologists and conservationists alike.

Frank E. Zachos

1Species concepts and species delimitation in mammals

1.1Introduction

Few topics in biology are as contentious and vexed as the ‘species problem’—a group of issues relating to what biologists over the past centuries have been calling species, such as Do species exist? What is a species? Is there a one-size-fits-all species concept applicable in a satisfactory manner to all groups of living beings? How can species be delimited from one another, and is this possible in an objective way? Debates on these questions can be intense, reflecting the importance of the species as a conceptual unit in biology and because every biologist has (or feels he or she should have) some idea of what makes a species. Each single question given above to circumscribe the species problem is in itself worth a whole treatise, and a detailed, let alone complete, discussion is far beyond the scope of this chapter. Yet, mammalian taxonomy is not only deeply affected by the answers to these questions but has also triggered some of the recent debates concerning species concepts. The present chapter highlights and summarizes these developments with a particular focus on mammal species, points out strengths and weaknesses of different taxonomic approaches, and also briefly addresses the practical consequences of our taxonomic decisions.

1.2Species concepts — a short outline

In this section, I will only highlight a few aspects and basic ideas of the general debate inasmuch as they are relevant to the more particular issues of this chapter. This will necessarily be short and at times superficial; for a more detailed discussion of the historical, philosophical, and theoretical aspects of species concepts, there are a number of books and review articles to which I refer the interested reader and from which I have drawn in the following discussion (e.g., Wilson 1999, Wheeler and Meier 2000, Ghiselin 2001, Mallet 2001, Stamos 2003, Rieppel 2007, Wilkins 2009a,b, 2018, Richards 2010, Kunz 2012, Zachos 2016, 2018, and references therein).

1.2.1Terminology

There are a few terminological issues in the species debate that are worth clarifying up front:

Species taxa vs. the species category. There is a fundamental difference between a species taxon, e.g., Homo sapiens, and the species as a category (and rank), i.e., a general unit with certain properties that we use to define what we call species. It is the latter that is aimed at in the definitions of the various species concepts. Species taxa are historical entities; they come into being through speciation and they cease to exist when they become extinct (or, perhaps, when they give rise to daughter species). Philosophically speaking, species taxa are individuals (Ghiselin 1974), and the various organisms that make up a species (all human beings in the case of H. sapiens) are parts of that individual, just like all the kings and queens and their immediate relatives are parts of a royal dynasty. The species category, on the contrary, is what philosophers call a class, a group whose members (which are usually called elements) show the defining characters of that class. These characters are essential, i.e., they are both necessary and sufficient: the class of red triangles is defined by color (red) and shape (triangular)—all its elements are red and triangular, and all red triangular objects are members of that class. Although individuals are bound in space and time (they have a beginning and an end), classes do not have any spatiotemporal limits—they exist regardless of space and time. H. sapiens is an ephemeral historical entity; the class of red triangles is not. When the last human dies, H. sapiens will no longer exist, and it will never again exist; the class of red triangles can be empty (no red triangles in the universe), but it can never cease to exist. When all life on earth dies out, none of the species taxa (humans, tigers, dandelions) will ever exist again, but if life evolves again (on earth or elsewhere), entities (i.e., groups of organisms) might come into existence that fall under one or more of our definitions of the species category.

For example, there may be least inclusive monophyletic groups of organisms (one version of the phylogenetic species concept [PSC]) or groups of organisms that produce fertile offspring among each other but infertile or no offspring with other such groups (biological species concept [BSC]). An analogy for the difference between the species taxa and the species category is that of a particular neighbor and neighbors in general: my neighbor Mr. Miller is an individual and, in the analogy, equivalent to the species taxon, whereas neighbors in general, defined as people living next door, are equivalent to the species category. From this, another difference becomes clear: the species category can be defined (as in the various species concepts), but species taxa can only be pointed out ostensively, and their names are therefore proper names (‘Mr. Miller’). The same is true for higher taxa: one can define the class of higher taxa as monophyla (a group containing a stem species and all and only its descendants), but each actual monophylum in the Tree of Life, Mammalia for example, is an individual and can only be discovered and delimited through phylogenetic analysis, as an actual instance of the class of monophyla by pointing out (or rather inferring) a stem species and all its evolutionary descendants. The fact that species taxa cannot be defined means that there is no character that is necessary and sufficient to make an organism part of a certain species. Morphological or genetic definitions of species taxa are, strictly speaking, invalid. A tiger that is born without stripes is still a tiger, and that holds for any and every character that one might choose to try and define a species taxon. An organism is not part of a species taxon due to its characters but only due to it being part of the historical entity that came into being in a speciation event at some particular point in time. This directly leads to the next important distinction, that of ontology and operationalism.

Ontology/definition vs. operationalism/identification. The difference between these two with respect to species concepts is a fundamental one, and the solution (in theory) of the species problem as presented below is a direct consequence of recognizing this difference. Ontology is about what things are and, consequently, how they are defined; operationalism (in this context) means being applicable and useful in practice. In the species debate, operational species ‘concepts’ (or rather criteria, see below) are those that help us identify species. Choosing human siblings as an analogy, the difference immediately becomes clear. Siblings are humans who share the same parents. This is a definition of what siblings are, but it is often useless in identifying siblings because ‘having the same parents’ is usually not directly observable. There are many ways of identifying siblings, though, morphologically and genetically. However, to say siblings are humans who share (on average) 50% of their genome is, strictly speaking, wrong. Apart from the fact that the same is true of parents and their children, it is not what makes two people siblings but simply a consequence of their being siblings that we use to identify them as such.

1.2.2A hierarchy of species concepts

There are more than 30 published species concepts (Mayden 1997, http://scienceblogs.com/evolvingthoughts/2006/10/01/a-list-of-26-species-concepts/ by J. S. Wilkins, Wilkins 2009b, 2018, Appendix B, Zachos 2016, chapter 4.). Identifying the best of those 30 concepts naturally depends on the purpose to which a species concept is put. It was probably Mayden (1997) who first explicitly distinguished two conceptual levels in species concepts. According to this view – the division-of-conceptual-labor solution to the species problem according to Richards (2010) –there is only one primary species concept that gives a true definition of what species ontologically are, whereas all the others function as secondary operational concepts to identify species, i.e., as criteria that must be fulfilled to satisfy the definition of the primary concept. The single primary species concept, according to Mayden, is the evolutionary species concept (ESC) that defines species as lineages of ancestraldescendant populations that evolve independently of other such lineages (Simpson 1951, 1961, Wiley 1978, Wiley and Mayden 2000a,b, and c; see Tab. 1.1). The ESC has often been criticized for not being operational, but ironically, this is exactly what makes it (ontologically) superior to all the other concepts. The same line of reasoning can be found in a number of publications by Kevin de Queiroz under the names of General Lineage Concept (de Queiroz 1998, 1999) and Unified Species Concept (de Queiroz 2005, 2007)1. Again, separately evolving population (or meta-population) lineages are viewed as common to all species concepts, and the secondary concepts or criteria only highlight certain thresholds that will be crossed sooner or later by diverging lineages, e.g., occupying different niches (Ecological Species Concept), producing sterile hybrids (BSC), being reciprocally monophyletic (monophyly version of the PSC), etc. (see Fig. 5.4 in de Queiroz 1998 and Fig. 5.2 in Zachos 2016). Viewed in this light, the existence of so many (secondary) species concepts that function as operational criteria to identify independent population lineages (= species as defined by the primary ESC) is actually an advantage rather than a nuisance. From this, it becomes clear that all species concepts are based on biological realities. Although they may be inconsistent as practiced by some of their adherents or not applicable to all taxa, they cannot simply be wrong. The decisive question is whether the biological reality a certain species concept highlights (sterile hybrids, diagnosable differences, separate niches, etc.) is what we think deserves the label ‘species’. Below, I argue that this is ultimately a question of convention.

Tab. 1.1: Definitions of selected species concepts dealt with in this chapter. For all of the listed concepts, more definitions than the ones given here exist, although differences are subtle and not relevant for the present discussion. Dobzhansky (1935) quoted from Wilkins (2009b). * The reference to populations in the definition of Wiley and Mayden (2000a) compared to that of Wiley (1978) was dropped to include asexual taxa. For a longer list of the 30+ published species concepts and their definitions, see chapter 4 of Zachos (2016) and Appendix B in Wilkins (2018).

Species concept	Species definition	Reference
Evolutionary species concept	“a lineage of ancestral descendant populations which maintains its identity from other such lineages and which has its own evolutionary tendencies and historical fate”	Wiley (1978)
	“an entity composed of organisms that maintains its identity from other such entities through time and over space and that has its own independent evolutionary fate and historical tendencies”*	Wiley and Mayden (2000a)
Biological species concept	“a group of individuals fully fertile inter se, but barred from interbreeding with other similar groups by its physiological properties (producing either incompatibility of parents, or sterility of the hybrids, or both)”	Dobhzansky (1935)
	“groups of interbreeding natural populations that are reproductively isolated from other such groups. Alternatively, one can say that a biological species is a reproductively cohesive assemblage of populations”	Mayr (2000)
Genetic species concept	“a group of genetically compatible interbreeding natural populations that is genetically isolated from other such groups”	Baker and Bradley (2006)
Phylogenetic species concept (diagnosability version)	“the smallest diagnosable cluster of individual organisms within which there is a parental pattern of ancestry and descent”	Cracraft (1983)
	“the smallest aggregation of (sexual) populations or (asexual) lineages diagnosable by a unique combination of character states”	Wheeler and Platnick (2000a)
Phylogenetic species concept (monophyly version)	“the smallest monophyletic groups deemed worthy of formal recognition, because of the amount of support for their monophyly and/or because of their importance in biological processes operating on the lineage in question”	Mishler and Theriot (2000a)

Mayden (1997) presents an analogy from cladistics to illustrate the conceptual difference between the primary and the secondary species concepts: the primary concept, the ESC, is equivalent to the concept of a monophylum that is not directly observable; the secondary concepts function as identification criteria and correspond to the search for synapomorphies that are used to identify or infer monophyletic groups. Unfortunately, this division-of-conceptual-labor solution (Richards 2010) to the species problem pertains only to the theoretical aspects of the species problem. The challenge lies in the realm of taxonomic practice where one has to make concrete decisions whether two populations or groups of populations are one or two species, i.e., it is not so much the definition of the species category, but rather the delimitation of species taxa that is most contentious (and most difficult).

1.2.3Taxonomy’s basic problems: continuous evolution and the fractal nature of the Tree of Life

The species problem for practicing biologists is mainly a problem of delimitation. This holds regardless of the underlying species concept, as boundaries will ...

Table of contents

• Cover
• Title Page
• Copyright
• Preface
• Contents
• List of contributing authors
• 1 Species concepts and species delimitation in mammals
• 2 Chromosomes and speciation in mammals
• 3 Taxonomy, trees, and truth in historical mammalogy
• 4 Mammalian embryology and organogenesis
• 5 Non-Mammalian synapsids: the deep roots of the mammalian family tree
• 6 Mesozoic mammals — early mammalian diversity and ecomorphological adaptations
• 7 Diversity and relationships within crown Mammalia
• 8 Mammal extinction risk and conservation: patterns, threats, and management
• Index