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Impacts of taxonomic inertia for the conservation of African ungulate diversity: An overview

April 2017
Biological reviews of the Cambridge Philosophical Society 93(Suppl):0-0

DOI:10.1111/brv.12335

Authors:

Spartaco Gippoliti

Società Italiana per la Storia della Fauna "Giuseppe Altobello"

Fenton Peter David Cotterill

Stellenbosch University

Dietmar Zinner

German Primate Center

We review the state of African ungulate taxonomy over the last 120 years, with an emphasis on the introduction of the polytypic species concept and the discipline's general neglect since the middle of the 20th century. We single out negative consequences of 'orthodox' taxonomy, highlighting numerous cases of neglect of threatened lineages, unsound translocations that led to lineage introgression, and cases of maladaptation to local conditions including parasitic infections. Additionally, several captive breeding programmes have been hampered by chromosome rearrangements caused by involuntary lineage mixing. We advocate that specimen-based taxonomy should regain its keystone role in mammal research and conservation biology, with its scientific values augmented with genomic evidence. While integration with molecular biology, ecology and behaviour is needed for a full understanding of ungulate alpha diversity, we stress that morphological diversity has been neglected despite its tremendous practical importance for some groups of 'utilizers' such as trophy hunters, wildlife tourists and conservationists. We conclude that there is no evidence that purported 'taxonomic inflation' has adverse effects on ungulate conservation: rather, it is taxonomic inertia that has such adverse effects. We stress that sound science, founded on robust taxonomy, should underpin effective sustainable management (hunting, ranching, captive breeding and reintroduction programmes) of this unique African natural resource.

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Biol. Rev. (2017), pp. 000–000. 1

doi: 10.1111/brv.12335

Impacts of taxonomic inertia for the

conservation of African ungulate diversity:

an overview

Spartaco Gippoliti1, Fenton P. D. Cotterill2, Dietmar Zinner3,∗and Colin P. Groves4

1Societ`a Italiana di Storia della Fauna ‘G. Altobello’ Viale Liegi 48, 00198 Roma, Italy

2Geoecodynamics Research Hub, Department of Earth Sciences, University of Stellenbosch, Stellenbosch 7602, South Africa

3Cognitive Ethology Laboratory, German Primate Center, 37077 G¨ottingen, Germany

4School of Archaeology & Anthropology, Australian National University, Canberra, Australia

ABSTRACT

We review the state of African ungulate taxonomy over the last 120 years, with an emphasis on the introduction of

the polytypic species concept and the discipline’s general neglect since the middle of the 20th century. We single out

negative consequences of ‘orthodox’ taxonomy, highlighting numerous cases of neglect of threatened lineages, unsound

translocations that led to lineage introgression, and cases of maladaptation to local conditions including parasitic

infections. Additionally, several captive breeding programmes have been hampered by chromosome rearrangements

caused by involuntary lineage mixing. We advocate that specimen-based taxonomy should regain its keystone role

in mammal research and conservation biology, with its scientiﬁc values augmented with genomic evidence. While

integration with molecular biology, ecology and behaviour is needed for a full understanding of ungulate alpha diversity,

we stress that morphological diversity has been neglected despite its tremendous practical importance for some groups

of ‘utilizers’ such as trophy hunters, wildlife tourists and conservationists. We conclude that there is no evidence that

purported ‘taxonomic inﬂation’ has adverse effects on ungulate conservation: rather, it is taxonomic inertia that has

such adverse effects. We stress that sound science, founded on robust taxonomy, should underpin effective sustainable

management (hunting, ranching, captive breeding and reintroduction programmes) of this unique African natural

resource.

Key words: conservation, morphological diversity, hybridization, phylogenetic species concept, extinct taxa, sustainable

utilization.

CONTENTS

I. Introduction .............................................................................................. 2

II. Historical perspective on ungulate taxonomy in Africa ................................................... 2

(1) The genesis of ungulate taxonomy ................................................................... 2

(2) Molecular contemporary approaches ................................................................. 4

(3) Why ‘taxonomic inﬂation’ is a misnomer ............................................................. 4

III. Taxonomic inﬂation and conservation ................................................................... 6

IV. Translocation ‘rescue’ and conservation genetics ......................................................... 7

V. The role of hybridization in species concepts and conservation .......................................... 9

VI. How can a ‘new alpha taxonomy’ support conservation? ................................................ 10

(1) Forgotten taxa, forgotten hotspots .................................................................... 10

(2) Taxonomic impacts on the wildlife industry and sustainable conservation ........................... 10

(3) How precise and accurate taxonomy informs a hierarchical conservation strategy ................... 11

VII. Conclusions .............................................................................................. 12

VIII. Acknowledgements ....................................................................................... 12

IX. References ................................................................................................ 12

* Address for correspondence (Tel: +49 551 3851129; Fax: +49 551 3851372; E-mail: DZinner@dpz.eu).

2S. Gippoliti and others

I. INTRODUCTION

Conservation biology requires taxonomy for sound scientiﬁc

guidance. Taxonomic errors have negative impacts on

accurate and precise knowledge of species diversity; these

errors can mislead conservation evaluations and misinform

characterizations of biogeographical history (Adams, 1998;

Bernardo, 2011; Cotterill et al., 2014). The taxonomic

impediment (Hoagland, 1996) compounds these challenges,

so that better surveyed taxa – pertinently vertebrates – are

relied on as surrogate indicators to assess biodiversity,

notably in gap analyses evaluating protected area coverage.

Moreover, conservation assessments increasingly employ

estimates of phylogenetic distinctiveness (PD) to characterize

historical attributes of taxa to identify biodiversity hotspots.

PD estimates expand the traditional focus beyond

quantifying extant population diversity to incorporate

evolutionary histories of biota across landscapes and

continents (King, 2009).

Remarkably, and notwithstanding earlier revisions of a few

species complexes (Cotterill, 2003a,b, 2005), until recently

the classiﬁcation of ungulates (hoofed mammals belonging to

the orders Artiodactyla and Perissodactyla) remained almost

unchanged from the middle of the 20th century. We here use

the term ‘taxonomic inertia’ to describe this persistence of

incomplete knowledge of biodiversity. Fortunately, the tax-

onomy of ungulates underwent wholesale revision recently

(Groves & Grubb, 2011; Groves & Leslie, 2011) leading

to a considerable increase in the number of recognized

species. Interestingly, this revised classiﬁcation systematically

employs the phylogenetic species concept (PSC) to opera-

tionalize the evolutionary species concept (ESC) [the former

name for the general lineage concept (GLC) of de Queiroz

(1999)]. The application of the ESC has been criticized as

‘taxonomic inﬂation’ (a term ﬁrst used by Isaac, Mallet &

Mace, 2004) in recognizing too many false species (Type

I errors) (Cotterill et al., 2014). These criticisms invoke two

main issues: ﬁrst, recognizing ‘too many species’ has negative

consequences for conservation biology in that it impedes

human-assisted gene ﬂow (e.g. through restocking programs)

between threatened ‘populations’, when the latter are consid-

ered to be distinct species (Frankham et al., 2012; Heller et al.,

2013; Zachos et al., 2013a,b). Second, given insufﬁcient fund-

ing for biodiversity conservation, an increase in the number

of recognized species reduces the resources available per

threatened species and thus aggravates the ‘agony of choice’

for conservation planners and managers (Isaac et al., 2004;

Collen et al., 2011). Respondents to both criticisms argue that

understanding mammalian diversity must be guided by the

best available scientiﬁc framework within the available evi-

dence, and condemn artiﬁcial lumping of species because it

undermines biodiversity assessments, especially where plan-

ners rely on recognized species of ungulates as surrogate

indicators and/or ﬂagships in conservation planning (Gip-

politi, Cotterill & Groves, 2013; Cotterill et al., 2014).

Taxonomic inertia raises critical questions. What are its

impacts? In particular, how has taxonomic inertia inﬂuenced

not just past decisions but prevailing policy? And for the

ungulates, why has this debate been so delayed, compared

to the other main branches of vertebrate taxonomy, and

what are the consequences of this for understanding African

ungulate diversity, a unique heritage of this continent?

Here we review the history of ungulate taxonomy

to highlight how taxonomic inertia has propagated the

remarkable prevalence and persistence of taxonomic errors.

Presenting this long-overdue historical context explicates the

polarized points of view that shaped the major taxonomic

syntheses of African ungulates over the last 120 years. These

trends and tensions in taxonomic knowledge further (i)

distinguish between taxonomic revisions versus reviews, and

(ii) underscore the fundamental roles of available hypodigms

on which derived taxonomies ultimately stand or fall. Above

all, we show that impacts of taxonomic errors on conservation

are hard-hitting, and we highlight problems exacerbated by

the mixing of different populations of African ungulates,

in the wild and the semi-wild as well as in captivity.

These undermine the credibility of repeated translocations

of ungulate ‘species’.

II. HISTORICAL PERSPECTIVE ON UNGULATE

TAXONOMY IN AFRICA

(1) The genesis of ungulate taxonomy

Until the end of the 20th century, an established consensus

believed that the living African ungulates comprised 95

recognized species, three of which became extinct recently

(summarized in the compilation of Corbet & Hill, 1986),

and it followed that the goal to maintain the diversity of

ungulate species in Africa was not a ‘mission impossible’. This

‘orthodox’ taxonomy, originating in reviews and checklists

(not true taxonomic revisions) of the 1930s, 1940s and 1950s,

had come to be perceived as deﬁnitive by the scientiﬁc

community. This tacit belief coincided with a general decline

of interest in researching mammal collections, especially in

Western European museums. Here, we deﬁne ‘orthodox’

taxonomy as the classiﬁcation derived from the taxonomic

reviews of Allen (1939); Ellerman & Morrison-Scott

(1951) and Ellerman, Morrison-Scott & Hayman (1953),

which classiﬁed previously described mammals using a

polytypic species concept [biological species concept (BSC)

or morphological species concept (MSC)]. Over the

following decades, and despite the addition of little, if

any, empirical evidence, the taxonomic arrangements in all

three monographs have been unquestioningly accepted and

utilized, and often perceived as ‘deﬁnitive’ by users, leading

to decades of taxonomic inertia (Gippoliti & Groves, 2012).

The low contemporary appeal of mammalian taxonomy

meant that few biologists scrutinized ungulate diversity,

unlike the attention paid to the more speciose small mammals

such as Rodentia and Chiroptera, even when new potential

material and data were available. Thus Cuneo (1965), for

example, while describing the breeding at Naples Zoo of

Taxonomic inertia and ungulate conservation 3

Abyssinian klipspringers Oreotragus saltatrixoides,reportedthat

of the four founder individuals, the two received from the

Asmara–Keren area had a chestnut-grey pelage, while the

two from Senafe had a grey-brown pelage. This remarkable

observation – on antelopes originating from within the same

country, within a distance of less than 150 km – corroborates

evidence of geomorphological controls on diversiﬁcation of

Ethiopian large mammals (cf . Gippoliti, 2010). It is unlikely

that any of these Naples klipspringer founders was deposited

and appropriately labelled in a museum after death – yet

another example of taxonomic neglect (Cotterill & Foissner,

2010).

In the 1980s, the ﬁrst quantitative genetic studies identiﬁed

an important potential problem for conservation biology.

Evaluations of captive populations (such as those of dorcas

gazelle Gazella dorcas) revealed deﬁcient genetic variation and

heterozygosity, highlighting potentially insidious inbreeding

depression (Ralls, Brugger & Glick, 1980). This study served

to reinforce the prevailing concept of ‘biological species’,

and the conclusion was drawn that the interbreeding

of geographically separated populations – purportedly of

the same species – would increase genetic variation to

minimize the negative effects of inbreeding (Frankham

et al., 2012). While Speke’s gazelles Gazella spekei were used

as a model for the elimination of inbreeding depression

from a small captive stock (Templeton & Read, 1998),

another African mammal, the cheetah Acinonyx jubatus,

was found to exhibit apparently abnormally low genetic

diversity (O’Brien et al., 1985), and in this case interbreeding

between southern and eastern African individuals was

suggested as a possible countermeasure (irrespective of

potential outbreeding depression). Considered in hindsight,

preliminary population genetics data together with a

simplistic understanding of the small-population paradigm

(cf . Caughley, 1994) not only exerted a strong inﬂuence

on thinking among conservation professionals, but also

moulded policies toward the perceived sustainability of

animal populations – not only in ex situ situations but also in

protected areas. The case of dwindling species has received

high-proﬁle attention.

Signiﬁcantly, the historical trend towards lumping

ungulate species has been compounded by abuse of the

subspecies category. Perhaps this was favoured by the

impressive ﬂood of mostly spurious ‘species’ by some

late-19th century taxonomists such as Paul Matschie in

Berlin, which were often based on single individuals as well as

on metaphysical theories about the geographical distribution

of species along river basins rather than objective analyses

of variation of morphological characters. It was perhaps

as a counterbalance that other mammalian taxonomists

turned with enthusiasm to the trinomial, following the

lead of Lord Rothschild and his colleagues (Rothschild,

Hartert & Jordan, 1903; and see Mallet, 2004). Thus

Lydekker (1913, p. vi) already adopted ‘to a great extent

the principle of classing nearly related kinds of animals as

races of a single species rather than as distinct species ...’,

and, accordingly, classiﬁed the African buffaloes as a single

species, Bos [now Syncerus] caffer, with 21 subspecies. Ernst

Schwarz followed the same path of simpliﬁcation at the

species level – as in his paper on duikers and in his otherwise

seminal paper on Alcelaphus (Schwarz, 1914; Ruxton &

Schwarz, 1929). Rothschild himself contributed to the

spread of the trinomial in mammalian taxonomy, describing

numerous new ‘races’ (meaning subspecies) of ungulates (e.g.

Rothschild, 1921). It is possible that accepting subspecies

in a polytypic species served to lower the responsibility

for the taxonomist’s decision, but it is interesting that

already in 1916 this trend to recognize too many ungulate

subspecies despite only one (or few) specimens, and without

valid morphological characters, was criticized by some (e.g.

Camerano, 1916). As a taxonomic category, the subspecies

concept became a panacea to deal with problematic

situations: especially to characterize differing patterns of

morphological variation in (apparently) closely related

populations. In reality, conversely to the polytypic species

ideal, such variation could represent a population within a

metapopulation or a divergent lineage lacking unambiguous

evidence (morphological at least) of distinct evolutionary

independence.

In important respects, Schwarz was pioneering an

evolutionary approach in mammal taxonomy, especially in

his Alcelaphus paper (Ruxton & Schwarz, 1929), which was

part of a series entitled Stages in the Evolution of Species.After

publication of the inﬂuential books of Dobzhansky (1937);

Huxley (1940) and Mayr (1942) advocating the BSC, and

following the lead of Allen (1939), mammalogists at the then

British Museum (Natural History) seemed to take it as their

duty to revise the mammal checklists of the Old World

mammals in light of the New Systematics and the BSC

(Ellerman & Morrison-Scott, 1951; Ellerman et al., 1953).

Judging from at least two critical book reviews (Handley,

1954; Ansell, 1958a), the immediate response to Ellerman

and colleagues was that they had gone too far in lumping

‘species’ of Old World mammals. One reviewer of their

Mammals of Southern Africa (Ellerman et al., 1953) observed:

‘‘Their ‘species’ is frequently equal to the ‘species group’

of American taxonomists. It often appears that to them the

criterion of conspeciﬁty is gross resemblance, demonstration

of intergradations is unnecessary, and broad overlap of

ranges of ‘subspecies’ is an unimportant detail’’ (Handley,

1954, p. 460).

For decades, until the molecular biology revolution, a

general neglect undermined characterization of challenging

and/or cryptic diversity at the species level in vertebrates.

It was compounded over the next half century, because

taxonomy became ‘out of fashion’ and museum-based

research programs became limited in number and scope,

especially in Western Europe. The widespread negative

trends across comparative biology over this period hit

taxonomy hardest – in what Brooks & McLennan (1999,

2002) term the ‘Eclipse of History’ (cf . Cotterill, 2016).

As a consequence of this dearth of studies of the major

museum collections of large mammals, non-specialists tended

to assume that the taxonomy of these groups was resolved

4S. Gippoliti and others

and deﬁnitive. Species boundaries were treated as ﬁrmly

set. Moreover, it was believed that little if any diversity

awaited discovery, especially of large mammals. Illustrative

of this viewpoint was the reduction to a care and maintenance

policy of the avian and mammalian collections of the Natural

History Museum in London after 1989, recounted by Fortey

(2008). Viewed today in the context of the prevailing scientiﬁc

paradigm, there were few tentative advances through the

latter half of the 20th century, and only a few descriptions

of new taxa, such as the Nigerian pygmy hippopotamus

Choeropsis liberiensis heslopi by Corbet (1969), occasionally

broke through this ominous stagnation.

Since the beginning of the 21st century, a number of

more easily recognizable, geographically isolated lineages

have been rehabilitated as distinct species. Thus, Grubb

(1993, 2005) recognized 100 and 101 species of African

ungulates, respectively, in the two editions of Mammal Species

of the World. In the meantime Cotterill (2000, 2003a,b, 2005)

questioned the validity of the BSC to describe ungulate

diversity in Africa; he advocated the ESC as the only

valid solution to discover and describe the true diversity

of African antelopes, and also reiterated major problems

and challenges in mammalogy identiﬁed decades earlier by

Ansell (1958b). Even if all data from ungulate collections

of the major museums were collated – assembled from

across the globe – their hypodigms remain inadequate.

This general lack of specimens continues to weaken

quantitative comparisons of inter-demic variation to

inform modern, geographically representative taxonomic

revisions.

(2) Molecular contemporary approaches

One might have expected molecular evidence to help

solve these taxonomic inadequacies. Instead, it appears

the challenges of characterizing ambiguous morphological

variation have endured for decades, despite the grand

promises of molecular genetics since the 1950s: ﬁrst

karyology, then electrophoresis and more recently estimates

of genetic variation from directly sequencing the genome.

The latter began with random ampliﬁcation of polymorphic

DNA (RAPD) and related restriction-enzyme comparative

mapping, then mitochondrial DNA sequencing, inaugurated

by Avise and collaborators in the late 1980s (Avise, 2000),

and most recently comparative genomics. The most recent

suite of methods enabled by high-throughput sequencing

methods – exempliﬁed in restriction site associated DNA

sequencing (RADSeq) (Ekblom & Galindo, 2011) – enables

hitherto unprecedented characterization of genomic

variation. RADSeq has begun to be used in generic revisions,

where it vindicates earlier estimates of the widespread

incidence of cryptic species. This is underscored by the

exemplary taxon sampling in a recent study of African

guenons, including many subspecies, synonymized decades

earlier; comprehensive genomic evidence evaluated using

RADSeq now demonstrates that these subspecies are

evolutionarily independent lineages (Guschanski et al., 2013).

Prior to the recent invention of high-throughput

sequencing, exempliﬁed in RADSeq, pioneering studies of

genetic diversity of the Bovidae (e.g. Arctander, Johansen &

Coutellac-Vreto, 1999; Matthee & Robinson, 1999; Alpers

et al., 2004; Lorenzen, Heller & Siegismund, 2012) relied on

mitochondrial DNA (mtDNA) variation and microsatellites

as genetic markers. With the exception of the continental

overview of the Tragelaphus scriptus and T. sylvaticus complexes

(Moodley & Bruford, 2007), these preserved the conservative

taxonomy of Allen (1939) and Ellerman et al. (1953). Actually,

uncritically or otherwise, these authors assumed the reality

of these ‘species’, and did not test species boundaries.

The common deﬁciency is the failure of these studies to

explicitly genotype topotypical populations of all described

subspecies; it is then impossible to anchor phylogeographical

ﬁndings on the known taxonomic framework. Nearly all

phylogeographers continue to evaluate ungulate diversity

under a polytypic species concept. This widespread failure

to evaluate species boundaries critically in an explicit

phylogenetic framework is strange, and raises questions

considering expansion of tree-thinking philosophy (sensu

O’Hara, 1988) into conservation theory (e.g. Erwin, 1991;

Vane-Wright, Humphries & Williams, 1991), and increasing

investments prioritizing characterization of the evolutionary

dimensions of biodiversity in biodiversity assessments and

policy (Mouquet et al., 2012).

(3) Why ‘taxonomic inﬂation’ is a misnomer

In contrast to the general belief among biologists

and conservation practitioners, our actual knowledge of

large mammal diversity is poor. Taxonomic inertia has

undermined a representative knowledge of ungulate diversity

for far too long. There is disquieting evidence that the

traditional ungulate taxonomy not only rests on remarkably

weak scientiﬁc foundations, but also that signiﬁcant diversity

is still unknown and underexplored. Over decades, these

repeated failures by professionals ﬂow from the artiﬁcial

classiﬁcation of poorly known evolutionarily distinct taxa

into single polytypic ‘species’. The number of genuine

taxonomic revisions that have been conducted on African

ungulates – in fact, on any ungulate genera at all – can be

counted on the ﬁngers of one hand. Moreover, in these

few cases hypodigms were limited, often based on only one

museum’s collection (almost invariably the Natural History

Museum, London). Critically evaluated against this complete

lack of revisionary work, it is clear that the term ‘taxonomic

inﬂation’ is a misnomer, at least as far as ungulates are

concerned: quite simply, there has been no taxonomy to

be inﬂated.

Most seriously, many mainstream conservation practition-

ers appear unaware of these realities. Park managers and zoo

directors alike assume that existing knowledge of ungulate

diversity is resolved. Thus no species remain unrecognized;

for surely, give or take adjustments of the ‘subspecies’ status

of a few populations, is it not true that species lists were com-

pleted decades back? Moreover, where their conservation

proﬁle is disregarded as just population segments, subspecies

Taxonomic inertia and ungulate conservation 5

Table 1. Summary of over a century of classiﬁcation of African ungulates revealing signiﬁcant shifts in recognized species diversity

Family/subfamily

Sclater & Thomas

(1894–1900)

Lydekker & Blaine

(1913–1916)

Allen

(1939)

Meester & Setzer

(1971)

Corbet & Hill

(1986)

Grubb

(2005)

Groves & Grubb

(2011)

Rhinocerotidae — 2 2 2 2 2 3

Equidae — 5 5 5 4 4 5

Suidae — 8 5 4 4 6 8

Hippopotamidae — 2 2 2 2 2 3

Tragulidae — 1 1 1 1 1 1

Girafﬁdae — 3 3 2 2 2 9

Cervidae — 1 1 1 1 1 1

Bovinae 14∗10 11 10 10 10 39

Cephalophini 20 33 18 16 17 18 41

Reduncini+18 12 10 9 9 9 24

Hippotragini 9 7 7 7 7 8 11

Alcelaphini 18 14 10 7 7 10 25

Aepycerotini 2 1 1 1 1 1 2

Antilopini 39 48 34 27 26 24 60

Caprini — 3 3 2 2 3 3

Total number 120 150 113 96 95 101 235

∗Does not include Syncerus.

+Includes Pelea (following Robinson et al., 2014).

are of negligible evolutionary importance (Corbet, 1997). We

argue that all ‘de facto’ factors such as these have motivated

zoos and wildlife authorities to mix supposedly ‘conspeciﬁc’

stocks both in situ and ex situ (but see Dathe, 1978).

Nothing less than a landmark taxonomic revision was

needed to galvanize attention to taxonomic inertia of the

ungulates. The incisive synthesis by Groves & Grubb (2011,

hereafter G&G) compiled revisions carried out through a

collective eight decades of research, within the strictures of

available hypodigms in museums. Remarkably, it has met

with not just surprise, but hostility, in antagonism against

doubling the recognized number of species of ungulates.

Unfortunately, too few critics appear to understand not only

the motivations but especially the empirical foundations

underpinning G&G. One line of criticism seized upon

weaknesses perceived in the PSC used to reclassify the

ungulates. The PSC was used explicitly as a workable proxy

for the ESC. The G&G revision considerably increased

the number of recognized species as highlighted by a

synthesis of how species diversity of African ungulates has

been evaluated over more than a century (Table 1). G&G

ﬁnally recognized 235 species of African ungulates after

studying unprecedented hypodigms of specimens (Cotterill

et al., 2014). Although one of the earliest species lists (Lydekker

& Blaine, 1913–1916) was already inﬂuenced by lumping,

it is, nonetheless, interesting to note how its total of 150

species dropped in subsequent years. This ﬁnally reached

a minimum with Corbet & Hill (1986) of only 95 African

ungulate species. Interestingly, the number of global primate

species followed a similar trend: decreasing from 532 in 1912

to only 180 in 1967 followed by an increase to 233 in 1993,

370 in 2001, and 480 in 2013 (Rylands & Mittermeier, 2014).

With the application of morphometric and genetic methods,

in combination with the PSC, we have learned more about

primate taxonomy and evolution in the 13 years following

Groves (2001) standard work on primate taxonomy than in

the 50 years preceding Groves’ book.

It is important to acknowledge that G&G is the precursor

and catalyst for much taxonomic work that remains

unﬁnished. This applies especially where hypodigms are

small, as the high prevalence of incomplete hypodigms

makes the assessments of many populations tentative.

These inadequate samples of populational variation of

many hypodigms of candidate ungulate taxa are a strident

indicator of severe gaps in knowledge of large mammal

diversity – poor representation in the available and/or

examined museum collections (cf . Reddy & D´

avolos, 2003).

For example, no oribi Ourebia sp. from north of the Juba

River, Somalia, generally ascribed to the taxon haggardi,have

been studied and the few existing museum specimens await

comparison against the population from southern Somalia

and coastal Kenya. Wide-ranging species, such as the bongo

Tragelaphus euryceros, are mostly known from old museum

specimens received from a tiny part of their range –despite

this species being nowadays highly prized by trophy hunters

in Central Africa. Sample sizes are invariably small and the

last original taxonomic work dates from the beginning of

the 20th century (Thomas, 1902). In a little-known paper on

the African buffalo in southern Somalia, Fagotto (1980)

reported the existence of two ‘types’; one lightly built,

with horns which never curve downwards below the

level of the skull base and resembling the taxon Syncerus

brachyceros, while the more massive form with horns that

curve considerably downwards points to afﬁnities with

S. caffer. Interestingly, this latter form is present from the

borders with Kenya to the lower Sheebeli River (Awai),

beyond which the lighter form predominates northwards

along the Sheebeli lower course. The small amount of

material available in Italian museums is not likely to

help us solve this taxonomic question. Similar cases are

6S. Gippoliti and others

certainly widespread but, belatedly, G&G have unlocked a

new scientiﬁc era in large-mammal taxonomy. Important

collections in southern African museums, especially the

rich collections in the Natural History Museum, Bulawayo

(NMZB), have yet to be comprehensively evaluated,

with the exception of Damaliscus lunatus and Kobus leche

species complexes studied by Cotterill (2003a,b, 2005) and

unpublished results on Kobus cf. vardoni and Hippotragus

(F. P. D. Cotterill, unpublished data). This Bulawayo

collection is complemented by signiﬁcant large mammal

collections in Pretoria (TM, Ditsong Museum), East London

(Amathole Museum), Cape Town (SAM, Izoko Museum)

and Zambia (Livingstone Museum), and smaller but still

signiﬁcant collections in the Kenya National Museum,

Nairobi, and the Institut Fondamental d’Afrique Noire

(IFAN), Dakar. Regrettably, it seems that the importance

of a national repository for natural history collections is

not receiving attention in several African countries. There

are ample possibilities for European museum collections to

contribute to taxonomic studies (e.g. D’Huart & Grubb,

2001; Gippoliti et al., 2014) but this requires a paradigm shift

in current perceptions of natural history museums and their

collections (Cotterill, 2016).

Finally, apart from the vast amount of morphological

data stored in museum collections, molecular studies offer

an opportunity to uncover much of the geographical and

temporal genetic variation held there. However, genetic

studies of historical museum specimens typically rely on

extracting highly degraded and chemically modiﬁed DNA

samples from skins, skulls or other dried samples. Until

recently, it was possible only to obtain short fragments of

DNA sequences using traditional polymerase chain reaction

(PCR) ampliﬁcation. Recently, however, approaches using

high-throughput next-generation sequencing to obtain

reliable genome-scale sequence data have been proposed

(e.g. Rowe et al., 2011). This allows obtaining data

for single-nucleotide polymorphisms (SNPs) or complete

mitochondrial genome sequences even from degraded

source materials. The biological material required can

be as little as 10 mg with high success rates of PCR

ampliﬁcation. This is particularly important when sampling

from museum specimens, as it avoids destructive tooth

or bone sampling (Wandeler, Hoeck & Keller, 2007;

Guschanski et al., 2013; see also Bi et al., 2013). Museum

collections allow genotyping of type specimens, as was

recently carried out for the lectotype of the Arabian gazelle

Gazella arabica consisting of a skull and skin, which led

to the discovery that it was of composite origin and only

the skin should be retained as the name-bearing specimen

(B¨

armann et al., 2013). Obviously it is now possible to sample

museum specimens belonging to extinct taxa/populations

to produce more-complete phylogeographic information

to resolve taxonomic issues concerning highly threatened

species. This has been done with the Nubian wild

ass Equus africanus (Kimura et al., 2010) and the

giant sable antelope Hippotragus niger variani (Themudo,

Ruﬁno & Campos, 2015).

III. TAXONOMIC INFLATION AND

CONSERVATION

Several prominent conservation geneticists who have

invested decades of research efforts to the identiﬁcation and

conservation of distinctive and often-threatened evolutionary

units (e.g. Frankham et al., 2012; Heller et al., 2013, 2014;

Zachos et al., 2013a,b) are strongly opposed to the shift in

mammal taxonomy resulting from adoption of the PSC

(Groves, 2001; Groves & Grubb, 2011). The rationale

underlying this criticism lies in concerns over dissipation of

conservation resources on populations traditionally lumped

into single ‘species’, using the BSC. Such opposition is

ironic given the contributions of these and other geneticists

to the uncovering of discrete lineages within traditionally

recognized species.

Underlying this criticism is the argument of Isaac et al.

(2004) that excessive taxonomic splitting impacts negatively

on macroecological research and conservation. First, we

should note that part of their problem lies in the current

biased application of ESC in mammalogy. At present we

have an ESC synthesis for Primates, Artiodactyla and

Perissodactyla while other orders, such as Hyracoidea,

remain classiﬁed in an overlumped BSC-based taxonomy.

This problem is attributed to the present period of transition,

not an underlying ﬂaw within the ESC itself.

Regarding the supposed negative effects of a PSC-based

taxonomy, we note that a survey by Morrison et al. (2009)

found no evidence for negative effects of taxonomic splitting

on conservation, but rather found the exact opposite: in

addition we highlight the dubious record of ‘orthodox’

taxonomy in creating long-standing ex situ problems, e.g. in

zoo breeding programs during the 20th century. Here the

legacy of ‘taxonomic inertia’ is manifested by overlooking

ﬁner scale diversity and the geographical origins of founder

populations, bequeathing chimerical stocks of zoo ungulates

of unknown and/or admixed evolutionary lineages. As a

potpourri of different populations, the ex situ conservation

status of these purported ‘species’ is disputable. For example,

two supposed subspecies of East African dikdik Madoqua

kirkii had different karyotypes and were found to produce

infertile offspring when interbred in zoos (Kumamoto,

Kingswood & Hugo, 1994; Cernohorska et al., 2011); there

are in fact four species, morphometrically distinguishable,

within what was lumped as M. kirkii, and skulls of dikdik

of known karyotype could easily be identiﬁed by being

ﬁtted in to this scheme (Groves & Grubb, 2011). A study

of the karyotypes of the North American zoo population

of suni Nesotragus moschatus found even greater chromosome

variability, with Kenyan animals (N. m. akeleyi) exhibiting

2N =56 and KwaZulu-Natal animals (N. m. zuluensis)2N

=52 (Kingswood et al., 1998). It was sensibly suggested that

these two ‘subspecies’ should be managed separately given

evidence of probable breeding problems in hybrids, and they

are now classiﬁed as different species by G&G. In another

study, heterozygosis for three chromosomal changes (centric

fusions) was invoked as causing high perinatal mortality in

Taxonomic inertia and ungulate conservation 7

captive Soemmering’s gazelles Gazella soemmeringi (now Nanger

soemmerringii) (Benirshke et al., 1984), although, in this case, it

is unclear whether chromosomal rearrangements correlate

with subspeciﬁc status and thus what the possible roles of

inbreeding and outbreeding in perinatal mortality might be

(see Steiner et al., 2016, who suggested a genetic and chro-

mosomal study of wild populations to clarify the relationship

between taxonomic status and chromosomal rearrangements

in Soemmering’s gazelles). There are at present not many

captive breeding programmes for small and medium-sized

ruminants representing the Antilopini, Cephalophini and

Tragulidae; so opportunities comprehensively to evaluate

effects of outbreeding remain severely limited. Nonetheless,

available data suggest that the karyotypic diversity of the

Bovidae is more similar to that of rodents than to other

large mammals such as carnivores (Kumamoto et al., 1999;

Pagacova et al., 2011; Robinson & Ropiquet, 2011).

Outbreeding depression (Storfer, 1999) is now recognized

to be as great a problem as inbreeding depression in wildlife

conservation and captive breeding programmes. Its negative

effects persist even after admixture of distant populations

of apparently monotypic species such as Arabian oryx Oryx

leucoryx (Marshall & Spalton, 2000). Pedigree analysis has

revealed outbreeding depression in captive populations of

Indian rhinoceros Rhinoceros unicornis representing separate

populations from Nepal and Assam (Zschokke & Baur,

2002); belatedly, these two genetically distinctive populations

are now acknowledged to be best managed separately

(Zschokke et al., 2011). Although similar cases of breeding

incompatibility likely exist in several other rhinoceros

populations in Africa and Asia, their classiﬁcation as

‘subspecies’ confers a dubious status on these populations.

This is most notorious when ‘just a subspecies’ is declared

extinct (Gippoliti et al., 2013). This is the case of the Nile

rhinoceros (northern white rhinoceros) Ceratotherium cottoni,

of which only three individuals are still living in captivity

and apparently none in the wild. The species rank accorded

by Groves, Fernando & Robovsk´y (2010) has been recently

challenged by Harley et al. (2016) fearing that the rescue

and conservation of C. cottoni through hybridization with

the southern white rhinoceros C. simus may be prevented

by taxonomic splitting; yet there is strong evidence that the

only female hybrid produced in Dvur Kralove Zoo showed

signs of outbreeding depression, never bred and was larger

and heavier than any other recorded female (Dvur Kralove

Zoo records). As evidenced by a recent proposal to manage

Sumatran and Bornean rhinoceros Dicerorhinus sumatrensis

as a single ‘management unit’ (Goossens et al., 2013), some

conservationists continue the dubious practice of overlooking

negative consequences of outbreeding depression. Note,

however, that the absence of any perceived negative effect

from introgression of two or more closely related taxa does

not constitute a criterion for their conspeciﬁcity.

The species of African ungulates rated as extinct or

near-extinct over the last two centuries makes sobering

reading (Table 2). Although the taxonomic status of

some of these taxa is still controversial, biogeographical,

morphological, and genetic evidence (where known)

suggests that these extinctions have extirpated considerable

phylogenetic diversity. Orthodox taxonomy stands out as

the propagator of several extinctions, especially in the past

half a century. Conspicuous losses of phylogenetic diversity

among wide-ranging African mammals are exempliﬁed by

the black rhinoceros Diceros spp. (Moodley et al., 2017).

The distinctively long-legged black rhino Diceros longipes

from the Chad region – presently recognised as Diceros

bicornis longipes – would certainly have received much greater

attention and conservation support had its morphological

and taxonomic distinctiveness been thoroughly investigated.

Furthermore, given the high value people place on rarity

(Angulo et al., 2009), this species should have constituted an

exceptional ﬂagship species for conservation in west-central

Africa, and an important focus for tourist attraction in a

region otherwise neglected.

The case of the Nubian wild ass Equus africanus stands

unique among all these extinctions. It was treated as one of

at least two subspecies (the other being the Somali wild ass

Equus somaliensis; see Groves & Smeenk, 2007 for a recent

synthesis), until the distinction of these lineages was confuted

after the mid 20th century. As a result the Nubian wild ass

practically disappeared from the scientiﬁc and conservation

literature (Gippoliti, 2014). Recent genetic studies seeking

to resolve the origin of donkeys Equus asinus genotyped old

museum specimens. These conﬁrm the distinctiveness of

the two taxa, highlighting the Nubian wild ass as ancestor

of the donkey (Kimura et al., 2010); it is perhaps not too

late to save this neglected species from extinction, as there

are at least a few individuals, now carefully protected,

persisting in south-eastern Egypt (Sultan Mos’ad, personal

communication).

IV. TRANSLOCATION ‘RESCUE’ AND

CONSERVATION GENETICS

Several critics of the PSC argue that small and declining

populations might be rescued through translocations from

other populations, but such conservation ‘rescue’ efforts are

undermined now that these populations are characterized

as distinct (Frankham et al., 2012; Zachos et al., 2013b;

Heller et al., 2014). Besides the failure to ﬁnd concrete

examples to support this fear of a (theoretical) conservation

hurdle, this argument overlooks the respective evolutionary

histories of populations lumped into single ‘species’, and runs

counter to the increasing role of phylogenetic knowledge

in informing conservation decisions. Moreover, the ﬁndings

of Heller, Okello & Siegismund (2010), on genetic drift

in Syncerus caffer, conﬁned in isolated protected areas of

Uganda and Kenya, clearly show that human-mediated

gene ﬂow can be pursued without breaking the deeper

phylogenetic barrier that has evolved along the Victoria Nile.

On the contrary, we know of a few cases of ecological and

behavioural disruptions following mixing of evolutionarily

divergent lineages. In a classic case, the translocation of

8S. Gippoliti and others

Table 2. Extinct and near-extinct African ungulates in recent history

Taxon English name Original range Notes

Dicerosbicornislongipes

∗Western black rhinoceros Nigeria, Cameroon, Central African

Republic (CAR)

Extinct 2012

Ceratotherium cottoni∗Nile rhinoceros W. Uganda, S. Sudan, Garamba NP

(Democratic Republic of Congo),

CAR, Chad

Three individuals of breeding age in

semi-captivity

Equus quagga quagga∗Quagga S and E Cape, Free State (S. Africa) Extinct 1872

Equus africanus∗Nubian wild ass N Eritrea, NE Sudan, SE Egypt Status uncertain, Gebel Elba, Egypt

and possibly in Sudan

Phacocoerus aethiopicus∗Cape warthog S. Cape (S. Africa) Extinct

Choeropsis heslopi∗Nigerian pygmy

hippopotamus

Niger Delta, Nigeria Probably extinct

Giraffa camelopardalis∗Nubian giraffe NW Kenya, Ethiopia, Eritrea, Uganda,

Sudan (E of Nile)

Survives patchily in Kenya, Uganda,

Sudan, far-western Ethiopia

Kobus robertsi∗Roberts’ lechwe NE Zambia Extinct by 1950s

Hippotragus leucophaeus Blaubok SW Cape, Free State†Extinct 1800 (1860 if Free State record

is valid)

Alcelaphus buselaphus∗Bubal hartebeest North Africa Extinct 1925

Alcelaphus tora∗Tora hartebeest Nubia and W Ethiopia Possibly extinct 2010

Damaliscus selousi∗Selous’ topi Uasin-Gishu plateau, Karamoja Extinct sometime after 1930

Eudorcas ruﬁna Red gazelle Algeria Extinct pre-1894

∗Denotes taxa not included in Turvey (2009).

†This information comes from a claim of an eyewitness report of what sounds like blaubok in the Free State, in 1858. See Groves & Grubb

(2011, p. 198).

three interbreeding members of the genus Capra (Capra

ibex,C. nubiana and C. aegagrus, the latter two at that time

considered subspecies of C. ibex) on the Tatra Mountains

failed because of a different birth seasonality (Templeton,

1986). Geist, O’Gara & Hoffmann (2000) discussed how

wapiti and European red deer (Cervus canadensis and Cervus

elaphus species complexes) differ in their respective habitat

requirements and behavioural ecology, suggesting that

interbreeding can be advantageous only in semi-captive

situations. Such cases imply that the concern expressed by

several researchers (Frankham et al., 2012; Heller et al., 2013;

Zachos et al., 2013a,b) over the conservation consequences

of adopting the PSC is misplaced and unwarranted.

Paradoxically, wealthier African countries, such as South

Africa, face the biggest problems in protecting their original

ungulate diversity due to a mix of liberalism in wildlife

management and unsound use of scientiﬁc knowledge;

taxonomic inertia apparently plays a role. It is true that

modern conservation biology recognizes the importance of

maintaining intraspeciﬁc diversity [evolutionarily signiﬁcant

units (ESUs), management units (MUs), subspecies] (Moritz,

1994; Crandall et al., 2000), yet such detailed attention is

often accorded only to a few species in particular regions,

mostly in North America or Australia (Haig et al., 2006;

Gippoliti & Amori, 2007). Most national legislations protect

species, and species are the mandatory focus of IUCN Red

List assessments (see www.iucnredlist.org). Identiﬁcation of

biodiversity hotspots or sub-hotspots is based on endemic

species distributions, not on the distribution of subspecies

or ESUs (Dubois, 2003). In the few cases where resources

are abundant, due attention should be paid to intraspeciﬁc

variability (e.g. lion Panthera leo;tigerPanthera tigris; gorilla

Gorilla spp.; Wilting et al., 2015; Bertola et al., 2016) but this is

the exception rather the rule. Even highly charismatic large

mammals receive very little attention from this point of view

(e.g. African elephant Loxodonta spp.; brown bear Ursus arctos:

see Gippoliti, 2016; Groves et al., 2016). The zoo community

has so far allowed the mixing of Sumatran and Bornean

elephants within continental Asian family groups, despite the

strong phylogeographic structure found in Elephas maximus

(S. Gippoliti, personal observation).

Although South Africa should urgently adopt new

regulations to limit ecological and genetic effects of ungulate

translocations in private reserves (Cousins, Sadler & Evans,

2010) with the aim of avoiding further negative consequences

for native biodiversity, this still seems far from being achieved.

Yet, adoption of an ESC-based taxonomy would be a

step in the right direction. For example, the only buffalo

native to South Africa remains Syncerus caffer, but the G&G

taxonomy restricts this species to the southern and eastern

African savannahs east of the Western Rift Valley, while

Central and Western buffaloes are recognised as belonging

to three distinct species (S. brachyceros,S. mathewsi and S.

nanus) and, as exotic species, their importation could be

easily regulated or even prevented. Unregulated wildlife

translocations had severe consequences in North America

and Europe (Champagnon et al., 2012), and we may easily

imagine negative impacts among ungulates in Africa.

In some cases translocations of rare ungulates become

cosmetic initiatives at best; this is the case for ‘sitatunga’

(Tragelaphus spekii complex) reintroduction in The Gambia.

In fact, the sitatungas west of the Dahomey Gap seem to

Taxonomic inertia and ungulate conservation 9

represent an undescribed, very-little-known potential species,

but apparently no data are available on the origin of

the four individuals released at Abuko in 1968 (Starin,

2000). The fact is that one consequence of taxonomic

inertia is that of dismissing the role of the whole discipline

of morphology-based taxonomy, which some believe is

superseded by phylogeographic molecular studies.

Transmission of new diseases or failure to acclimatize

to endemic diseases is another widespread problem

encountered in the management of translocated ungulate

populations (Melter, 1993; Nijhof et al., 2005), and often

neglected by population geneticists. Interestingly, Nijhof et al.

(2005) reported the case of a pair of roan antelope Hippotragus

equinus originating from Togo and Benin succumbing to a

Theilerosis infection after release on a game ranch in southern

Mpumalanga, South Africa. As Aiello et al. (2014) showed

with the desert tortoise Gopherus agassizii, translocations and

augmentation may disrupt existing resident disease dynamics

and initiate an outbreak that would effectively offset any

advantages accompanying the translocation.

The dramatic recovery of the (southern) white rhinoceros

Ceratotherium simum in Kwazulu-Natal [but see Rookmaaker

(2000) for a critical review of historical data] shows that

the paradigm of population genetic theory (see Caughley,

1994) has been overemphasized in conservation biology at

the expense of factors such as political stability and effective

management and protection. If this is true, the current

emphasis on gene ﬂow and human-mediated translocations

in ungulate conservation needs to be considered in a wider

perspective.

V. THE ROLE OF HYBRIDIZATION IN SPECIES

CONCEPTS AND CONSERVATION

In the past, interbreeding or hybridization between animal

species was assumed to be of negligible concern, not at

least because of a near-universal belief in the infallibility

of the BSC as the conceptual tool with which taxonomists

classiﬁed living diversity; thus fertile interbreeding taxa by

deﬁnition were regarded as belonging to a single species.

Thanks to progress in molecular methods over the last

decades, however, it has become obvious that gene ﬂow

between species has been widespread in the past, and

continues in the present, in various taxonomic groups (e.g.

Mallet, 2005; Arnold, 2008; Schwenk, Brede & Streit, 2008;

Zinner, Arnold & Roos, 2011). Following in the footsteps

of botanists, there is increasing interest among zoologists in

the role of hybridization and its evolutionary consequences,

ranging from zero gene ﬂow when F1 individuals are sterile

to complete admixture or hybrid speciation (Arnold, 1997;

Allendorf et al., 2001; Larsen, March´

an-Rivadeneira &

Baker, 2010; Abbott et al., 2013). Given that species delimita-

tion is not a simple endeavour, not least because no universal

deﬁnition of species is yet accepted, despite the arguments of

de Queiroz (2007) and others, gene ﬂow among taxa makes it

even more complicated. Hybridization can have signiﬁcant

conservation impacts, in particular when conservation

is species-based (Simberloff, 1996; Allendorf et al., 2001;

Fitzpatrick et al., 2015; van Wyk et al., 2017). Questions arise

about the worthiness for conservation of populations with

hybrid ancestry, with inherent problems in the legal treat-

ment of hybrid populations (Fitzpatrick et al., 2015; Richards

& Hobbs, 2015). Often a distinction is made between

‘natural’ and ‘human-caused’ hybridization, although in

many cases it remains unclear what proportion of contem-

porary hybridization can actually be attributed to direct

(e.g. purposely introduced species) or indirect (e.g. species

range expansion due to human-caused habitat alterations or

climate change) human activities (Mallet, 2005).

Molecular techniques can detect past introgressions that

shaped the evolutionary histories of lineages (Zinner, Arnold

& Roos, 2009; Green et al., 2010), yet such events have

not always been suspected on morphological grounds (but

see Ackermann & Bishop, 2010; Ackermann et al., 2010).

Accumulating evidence of gene ﬂow between both universally

recognized species, even of different genera [e.g. in primates

(Roos et al., 2011; Zinner et al., 2011); in bovids (Verkaar et al.,

2004; Rodríguez et al., 2009)], as well as between ‘subspecies’,

undermines the roots of the BSC with its emphasis on

reproductive isolation (Mallet, 2008). This evidence for

interspeciﬁc gene ﬂow makes it all the more difﬁcult to

single out what qualiﬁes as a true species, and why such

populations differ from those that comprise a hybrid swarm,

as Ruxton & Schwarz (1929) proposed decades earlier for

East African Alcelaphus.

After studying two specimens of hartebeests from

south-west Ethiopia, de Beaux (1943) proposed that, when

a hybrid population shows constant characters, it should be

recognized as a distinct taxonomic entity. In this speciﬁc case,

he proposed that Alcelaphus buselaphus neumanni (Rothschild)

should be accepted with the following synonymy: ‘Alcelaphus

buselaphus lelwel (Heuglin) ×Alcelaphus buselaphus tora (Gray)

Ruxton and Schwarz’. More recently, Ouma et al. (2011)

investigated the genetic status of putative hartebeest hybrids

in Kenya. With respect to the declining status of these

populations, they afﬁrmed that ‘ ... in many African

countries, including Kenya, where there has been little

mixing of populations by translocation, opportunities to

conserve ongoing evolutionary processes persist, and should

be pursued’ (Ouma et al., 2011, p. 146). A proposed hybrid

swarm from divergent caribou lineages (Rangifer tarandus

tarandus and R. tarandus caribou) is considered a conservation

target in Canada (McDevitt et al., 2009). These examples,

both old and recent, highlight the need to reconsider

the taxonomic and conservation implications when we

acknowledge that hybridization is an historical process.

Moreover, much greater attention should be paid to the

possible detrimental effects of wildlife translocations or the

further reduction of sympatric populations of closely related

taxa that may encounter increased incidence of hybridization

due to the absence of conspeciﬁc mates. Paradoxically,

ungulate managers have often had privileged opportunities

to study artiﬁcially introgressed populations, yet the

10 S. Gippoliti and others

intricacies of natural evolutionary trajectories receive little

attention.

The complexity of conservation in cases of hybridization

becomes clear where human activities induce introgression

directly or indirectly, as summarized above (see also

Allendorf et al., 2001). The intentional or unintentional

introduction of closely related non-indigenous species may

lead to hybridization. Similarly, reduced population sizes

of related sympatric or parapatric species (through hunting

or other human impacts), might increase hybridization risk,

eventually leading to the extinction of one or both species

(Frankham, Ballou & Briscoe, 2002; Allendorf, Luikart

& Aitken, 2012; Fitzpatrick et al., 2015). In South Africa

there has been considerable concern about introgression of

southern blue wildebeest Connochaetes taurinus genes into the

local endemic black wildebeest Connochaetes gnou following

inopportune introductions of the former species into the

latter’s range (Grobler et al., 2011). But many more taxa

seem affected; some cases have been discussed in detail,

such as hybridizations between greater kudu and lowland

nyala Strepsiceros strepsiceros ×Tragelaphus angasi,orred

hartebeest and tsessebe Alcelaphus buselaphus ×Damaliscus

lunatus (Robinson et al., 2015). Furthermore, admixtured

populations of the Karoo and Kalahari springbok (Antidorcas

spp.) are purposely farmed for venison and trophy hunting

(Van Aswegen, Labuschagne & Grobler, 2012). Zebras

are also potentially affected by translocations in South

Africa (Castley, Boshoff & Kerley, 2001), with potentially

devastating effects for the now-recognized species Cape

mountain zebra Equus zebra and Hartmann’s zebra Equus

hartmannae. Introduction of scimitar-horned oryx Oryx dammah

into the historic range of gemsbok Oryx gazella puts the genetic

integrity of the latter at obvious risk (Castley et al., 2001).

Similarly, black-faced impalas Aepyceros petersi are also affected

by unregulated translocations (Green & Rothstein, 1998).

Introgression over the long term may reduce the abilities

of such species to adapt to present and future environmental

change (Rhymer & Simberloff, 1996) or may lead directly

to cytonuclear extinction (e.g. Gill, 1997; Cordingley et al.,

2009). So whether such evolutionarily distinct lineages

are termed species, ‘subspecies’, ESUs (Ryder, 1986), or

‘ecotypes’ (and so on), it is mandatory that we manage such

phylogenetically distinct lineages separately. In summary, the

negative impacts of outbreeding depression or introgression

underscore how the ESC (=PSC) derived taxonomy of

ungulates provides wide-ranging epistemological support to

biodiversity conservation. That this is evidently not the

current situation is clear from the widespread criticism of

G&G when they raised some subspecies to species rank.

VI. HOW CAN A ‘NEW ALPHA TAXONOMY’

SUPPORT CONSERVATION?

(1) Forgotten taxa, forgotten hotspots

Recent revisions of East African giraffes reveal that the

three recognized species are conﬁned to discrete ecoregions,

within which synchronization of birth season with rainfall

may be one mechanism that reduces gene ﬂow among giraffe

species (Thomassen et al., 2013). Belated recognition of the

real diversity of Giraffa (Brown et al., 2007; Groves & Grubb,

2011; Bock et al., 2014) exempliﬁes how the taxonomy of

these large mammals provides a framework to explore such

processes, provided it is founded on a lineage species concept.

The new alpha taxonomy of the ungulates provides essential

conservation support by highlighting biodiversity hotspots

previously overlooked, such as Katanga, the Zambezi and

the Nile watersheds (Gippoliti et al., 2013; Cotterill et al.,

2014). Equally, it is important to analyse responses of

African large mammals to climate change at the level of

phylogeographic lineages rather than orthodox ‘species’,

since this level of taxonomic precision is a prerequisite

to parse the focal variable in robust models (D’Amen,

Zimmermann & Pearman, 2013).

Although the increase in recognized alpha diversity of

clades might make ‘species conservation’ appear more

challenging to implement, this is vastly preferable to

the converse impacts of imprecise taxonomy fostered by

taxonomic inertia. An example of such impacts are species

allowed to slip into extinction unnoticed; such as the Tora

hartebeest Alcelaphus tora (Heckel et al., 2008), because it was

lumped as one of several subspecies of Alcelaphus buselaphus.

Taxonomic inertia has likewise conferred the dubious

distinction of complete, or near, extinction on such species

as the Nigerian pygmy hippopotamus Choeropsis heslopi,the

Queen of Sheba’s gazelle Gazella bilkis, the Nubian giraffe

Giraffa camelopardalis and the Nile rhinoceros Ceratotherium

cottoni. Arguably, their conservation status today could have

been vastly different had they been accorded species status,

or at least had their status openly debated. The same could be

said of species in imminent danger of following their slide to

extinction. Examples include the West African giraffe Giraffa

peralta, the Arava gazelle Gazella acaciae, the Upemba lechwe

Kobus anselli, and the Mt. Elgon red duiker Cephalophus fosteri.

(2) Taxonomic impacts on the wildlife industry and

sustainable conservation

African wild ungulates are worth many hundreds of millions

of US dollars as a source of protein for rural communities,

as hunting trophies, and as focal subjects of tourist attention

(Yasuoka, 2006; Lindsey, Roulet & Romanach, 2007; Nasi,

Taber & Van Vliet, 2011). Wild ungulates represent the

most notable component of bushmeat consumed in most

areas of the humid forest as well as the Zambezian savannahs

(Newing, 2001; Fusari & Carpaneto, 2006), and an important

source of income for alleviating poverty in rural communities

(de Merode, Homewood & Cowlishaw, 2004). Ironically we

know very little about the enduring escalating impacts of

bushmeat and other depredations on the true diversity of

ungulates. Local mismanagement is encouraged by orthodox

taxonomy, as exempliﬁed by the report into the decline of

blue duiker on Bioko Island (Grande-Vega et al., 2016).

According to G&G, the Bioko island blue duiker represents

an endemic species Philantomba melanorheus (Gray, 1846), but

Taxonomic inertia and ungulate conservation 11

Grande-Vega et al. (2016, p. 49) claimed that ‘The blue duiker

(Philantomba monticola) is an abundant and widely distributed

ungulate in continental sub-Saharan Africa’. Later they

emphasized that island populations may be more threatened

than others, but never used the name melanorheus in their

paper, even as a subspeciﬁc name. This is very different

from the attention paid to the endemic primate assemblage

of Bioko Island, with the fate of seven species/subspecies a

cause of great concern (Butynski, De Jong & Hearn, 2009).

Furthermore, recently, Sarasa (2013) highlighted that

previous analyses evaluating trophy prices and the

international hunting market are confounded by bias because

they overlooked intraspeciﬁc diversity of ‘traditional species’.

For example, among Spanish ibex, trophy prices for Capra

pyrenaica victoriae are much higher than Capra pyrenaica hispanica

because the latter has shorter horns. The different IUCN

conservation status of these two subspecies underscores why

the ‘biological species’ taxonomy undermines the accuracy

of comparative studies and conservation assessments.

We highlight the impact of taxonomic inertia on

the classiﬁcation – and equally on the conservation and

management – not only of ungulates but also other

charismatic African mega-herbivores, elephants of the

genus Loxodonta. Recognition of the true diversity of this

mega-herbivore obscures the high-proﬁle concern over the

plight of the African elephant, traditionally classiﬁed during

the period of taxonomic inertia as a single species. The reality

is that there are two lineages of unequivocal evolutionary

distinctiveness, often recognised by those working ﬁrst-hand

on the issue (Frade, 1931; Allen, 1936; Azzaroli, 1966).

This is not surprising, given that the genomic evidence

dates the divergence between savanna elephant Loxodonta

africana and forest elephant L. cyclotis to the Pliocene

(Rohland et al., 2010; Roca et al., 2015); crucially, it is L.

cyclotis that is most at risk from unsustainable anthropogenic

depredations, caused by habitat losses and poaching (Maisels

et al., 2013), but taxonomic inertia continues to obscure

its conservation plight. Ironically, morphological revisions

conclusively demonstrated the distinctiveness of the two

species nearly two decades ago (Grubb et al., 2000; Rohland

et al., 2010; Shetty & Vidya, 2011).

The role of African ungulates in the maintenance of

ecosystems, thus contributing ecosystem services to the

value of many millions, even billions of dollars, has only

begun to be estimated. The collapse of large mammal

populations in Central African forests following overhunting

for bushmeat may have long-term consequences for the

ecological integrity of the region (Abernethy et al., 2013).

Activities such as deforestation and hunting have direct

and indirect detrimental effects on ungulate biodiversity

in Africa, and a sound knowledge of alpha taxonomy is

asine qua non successfully to manage, conserve and study

this irreplaceable resource. Pre-G&G taxonomy set a poor

foundation that has misinformed and misled sustainable

management in too many cases. We have highlighted many

conspicuous failures in which the extreme tragedy – species

extinction – has occurred repeatedly. In the case of large

mammals, an outdated phenetic approach goes a long way to

explain this ‘domino-impact’ of weak science on conservation

policy and applied management (Cotterill et al., 2014).

We single out the persistence of a spurious alpha

taxonomy as the cause of biotic homogenization across

large regions of Africa, in the way that in some countries,

such as South Africa, translocations of various exotic or

extralimital ungulates is now considered a major risk to native

biodiversity (Castley et al., 2001; Spear & Chown, 2009), and

hybridization has seriously affected some threatened species

such as Connochaetes gnou and Damaliscus pygargus (van der Walt,

Nel & Hoelzel, 2013).

(3) How precise and accurate taxonomy informs a

hierarchical conservation strategy

A persistent challenge in conservation is to reconcile the

often disparate goals and challenges of single-species versus

ecosystem management, where the latter aims to maximize

biodiversity conservation. Ultimately, any single-species

conservation will fail in situ where ecosystem integrity is

ignored. This is where we highlight the increasing use in

conservation biology of decision-making processes relying on

phylogenetic diversity (PD) to identify and rank conservation

areas. It is no accident that the evolutionary lineage is the core

currency of PD calculation to diagnose biodiversity hotspots

and evolutionarily vibrant landscapes [as ﬁrst argued by

Erwin (1991) and see Mouquet et al. (2012)]. This approach

should ideally utilize both ancient and young lineages in

combination to map the most complete (i.e. representative)

range of unique landscape elements across the continent.

In the case of Africa, there have been major attempts

to identify biogeographical patterns using indicators of

evolutionary history of representative biota (e.g. Linder et al.,

2012), but the lack of primary information still weakens

this quest. G&G present a strong data set, where their

classiﬁed evolutionary species can be mapped out in the

most complete detail that locality data permit currently.

The strength of this approach is exempliﬁed by Moodley

& Bruford (2007) who integrated occurrence maps of the

lineages of the Tragelaphus scriptus and T. sylvaticus species

complexes into the matrix of African ecoregions. These

lineages of African bushbucks are demonstrated to provide an

informative proxy of palaeoecological afﬁnities, and at a ﬁner

scale a recent evaluation of endangered okapi (Okapia johnstoni)

reveals equally instructive evidence linking taxonomy to

ecoregions, especially where respective okapi lineages exhibit

congruence with other species (Stanton et al., 2014). Ironically

today, these ungulates diagnose high conservation values of

landscapes in which some indicator lineages appear to have

been extirpated.

Much work remains. We single out this evolutionary con-

servation strategy [the PD strategy] as a signiﬁcant – if not

the primary – practical strength of an ESC-based taxon-

omy in biodiversity conservation. Following King (2009),

application of the PSC at the population level minimizes

taxonomic errors, pertinently in applications informing in

situ planning and policy. At the ecosystem/landscape level,

12 S. Gippoliti and others

ungulates rank as textbook ﬂagship/umbrella species, and as

especially informative indicators, where their evolutionary

histories can inform biodiversity maps, and in turn diagnose

biodiversity hotspots. Indeed, G&G emphasize this in their

Introduction (G&G, p. 17) where they ﬂag some of the main

ecosystems revealed by local endemics of ungulates.

VII. CONCLUSIONS

(1) Science informs conservation, not the other way round.

In this respect, it is unfortunate that only within the past seven

years have conservation decision-makers been able to exploit

a sufﬁciently accurate and precise taxonomy of ungulate

diversity.

(2) In its role in revising biodiversity mapping, the new

taxonomy complements biogeographical data sets of other

indicators (pertinently the herpetofauna and avifauna), but

these data are still incomplete, and/or await electronic

databasing.

(3) Several salient lessons explain why the revision by G&G

has revealed so many new, and signiﬁcant, ﬁndings, issues,

and challenges for ungulate conservation.

(a) It highlights the application of modern taxonomic

methodology whereby high-quality knowledge feeds

conservation policy. This is notable where the identiﬁcation

of hitherto-unrecognised evolutionary species at the same

time identiﬁes overlooked conservation areas (e.g. Upemba

Swamps).

(b) Taxonomic assessments remain impossible without

tentelic records preserved in museums, especially as

the primary data of conservation concern are open to

independent checks, and focal studies, particularly using

new molecular methods.

underscores the primacy of a specimen-based taxonomy

over ‘expert’ opinions/assumptions. It is urgent that

collecting of specimens such as hunting trophies, bushmeat,

cropping exercises and pick-up specimens (e.g. road-killed

and predator-killed animals) becomes the norm, where

feasible in conservation terms, facilitated by government

and conservation authorities. Ultimately, we should aim to

collate and utilize all available material in world collections

to ﬁll gaps in taxonomic knowledge that can in turn be

translated into conservation strategies.

(d) Integration of morphology-based taxonomy has the

further merit of being potentially ‘palatable’ to exploiters

such as wildlife tourists (or indeed trophy hunters), and

serves as a vital mechanism to provide DNA to systematists

whose revisions are challenged by gaps in representation of

populations and/or geographical locations.

(e) As argued elsewhere at length (Cotterill et al., 2014)

these tentelic data that vouch for the data analysed in G&G

were classiﬁed employing modern methods of phylogenetic

systematics, and not least a species concept that replaces

the polytypic BSC with the lineage-based ESC (=GLC)

operationalized by the PSC. In short, G&G integrate

the complementary strengths of population-thinking and

tree-thinking.

(f) Contrary to Frankham et al. (2012), adoption of the

PSC has highly positive rather than negative consequences

for conservation science, especially in its characterization of

allopatric diversity.

(g) With improvements in precision and accuracy

(minimizing Type 2 and Type 3 taxonomic errors), G&G

sets the precedent to incorporate its classiﬁed lineages

into conservation-focused databases that integrate measures

of phylogenetic diversity to inform policy, especially in

implementing the Convention on Biological Diversity at

national, regional and global scales.

VIII. ACKNOWLEDGEMENTS

We thank Christian Roos, Giovanni Amori and Ernesto

Capanna for valuable discussions on earlier versions of the

paper. We also thank Eva B¨

armann and two anonymous

referees who identiﬁed weaknesses and helped to strengthen

the paper.

IX. REFERENCES

Abbott,R.,Albach,D.,Ansell,S.,Arntzen,J.W.,Baird,S.J.E.,Bierne,

N., Boughman,J.,Brelsford,A.,Buerkle,C.A.,Buggs,R.,Butlin,R.K.,

Dieckmann,U.,Eroukhmanoff, F., Grill, A., et al. (2013). Hybridization and

speciation. Journal of Evolutionary Biology 26, 229– 246.

Abernethy,K.A.,Coad,L.,Taylor,G.,Lee,M.E.&Maisels,F.(

2013).

Extent and ecological consequences of hunting in Central African rainforests in the

twenty-ﬁrst century. Philosophical Transactions of the Royal Society B 368, 20120303.

Ackermann,R.R.&Bishop,J.M.(

2010). Morphological and molecular evidence

reveals recent hybridization between gorilla taxa. Evolution 64, 271– 290.

Ackermann,R.R.,Brink,J.,Vrahimis,S.&De Klerk,B.(

2010). Hybrid

wildebeest (Artiodactyla: Bovidae) provide further evidence for shared signatures of

admixture in mammalian crania. South Africa Journal of Science 106,1–5.

Adams,B.J.(

1998). Species concepts and the evolutionary paradigm in modern

nematology. Journal of Nematology 30,1–21.

Aiello,C.M.,Nussear,K.E.,Walde,A.D.,Esque,T.C.,Emblidge,P.G.,

Sah,P.,Bansal,S.&Hudson,P.J.(

2014). Disease dynamics during wildlife

translocations: disruptions to the host population and potential consequences for

transmission in desert tortoise contact networks. Animal Conservation 17(Suppl), 27– 39.

Allen,G.M.(

1936). The forest elephant of Africa. Proceedings of the Academy of Natural

Sciences of Philadelphia 88, 15– 44.

Allen,G.M.(

1939). A checklist of African mammals. Bulletin of the Museum of

Comparative Zoology at Harvard 83, 1 –763.

Allendorf,F.W.,Leary, R. F., Spruell,P.&Weuburg,J.K.(

2001). The

problems with hybrids: setting conservation guidelines. Trends Ecology and Evolution

16, 613– 622.

Allendorf,F.W.,Luikart,G.H.&Aitken,S.N.(

2012). Conservation and the Genetics

of Populations. Second Edition. Wiley-Blackwell, Malden.

Alpers,D.L.,van Vuuren,B.J.,Arctander,P.&Robinson,T.J.(

2004).

Population genetic structure of the roan antelope (Hippotragus equinus) with suggestion

for conservation. Molecular Ecology 13, 1771– 1784.

Angulo,E.,Deves,A.L.,Saint Jalmes,M.&Courchamp,F.(

2009). Fatal

attraction: rare species in the spotlight. Proceedings of the Royal Society B 276, 1331 –1337.

Ansell,W.F.H.(

1958a). On the study of African mammals. Journal of Mammalogy 39,

577– 581.

Ansell,W.F.H.(

1958b). The need for better study collections of African ungulates.

Mammalia 22, 338– 347.

Arctander,P.,Johansen,C.&Coutellac-Vreto,M.A.(

1999). Phylogeography

of three closely related African bovids (tribe Alcelaphini). Molecular Biology and Evolution

16, 1724– 1739.

Arnold,M.L.(

1997). Natural Hybridization and Evolution. Oxford University Press,

Oxford.

Taxonomic inertia and ungulate conservation 13

Arnold,M.L.(2008). Reticulate Evolution and Humans. Origins and Ecology.Oxford

University Press, Oxford.

Avise,J.C.(

2000). Phylogeography: The History and Formation of Species. Harvard University

Press, Cambridge.

Azzaroli,A.(

1966). La valeur des caract`

eres crˆ

aniens dans la classiﬁcation des

elephants. Eclogae Geologicae Helvetiae 59, 541–564.

B¨

armann,E.V.,B¨

orner,S.,Erpenbeck,D.,R¨

ossner,G.E.,Hebel,C.&

W¨

orheide,G.(

2013). The curious case of Gazella arabica.Mammalian Biology 78,

220– 225.

de Beaux,O.(

1943). Mammalia. In Missione Biologica Sagan-Omo. Zoologia I (ed. E.

Zavattari), pp. 15– 57. Accademia d’Italia, Rome.

Benirshke,K.,Kumamoto,A.T.,Olsen,H.,Williams,M.M.&Oosterhuis,

J. (1984). On the chromosomes of Gazella soemmeringi Cretzshmar, 1826. Mammalian

Biology 49, 368– 373.

Bernardo,J.(

2011). A critical appraisal of the meaning and diagnosability of cryptic

evolutionary diversity, and its implications for conservation in the face of climate

change. In Climate Change, Ecology and Systematic (eds T. R. Hodkinson,M.B.Jones,

S. Waldren andJ.A.N.Parnell), pp. 380–438. Cambridge University Press,

Cambridge.

Bertola,L.D.,Jongbloed,H.,van der Gaag,K.J.,de Knijff,P.,Yamaguchi,

N., Hooghiemstra,H.,Bauer,H.,Henschel,P.,White,P.A.,Driscoll,

C. A., Tende,T.,Ottosson,U.,Saidu,Y.,Vrieling,K.&de Iongh,H.H.

(2016). Phylogeographic patterns in Africa and high resolution delineation of genetic

clades in the lion (Panthera leo). Scientiﬁc Reports 6, 30807. (https://doi.org/10.1038/

srep30807).

Bi,K.,Linderoth,T.,Vanderpool,D.,Good,J.M.,Nielsen,R.&Moritz,C.

(2013). Unlocking the vault: next generation museum population genomics. Molecular

Ecology 22, 6018– 6032.

Bock, F., Fennessy,J.,Bidon,T.,Tutehings,A.,Marais,A.,Deacon,F.

&Janke,A.(

2014). Mitochondrial sequences reveal a clear separation between

Angolan and South African giraffe along a cryptic rift valley. BMC Evolutionary

Biology 14, 219.

Brooks,D.R.&McLennan,D.A.(

1999). Species: turning a conundrum into a

research program. Journal of Nematology 31, 117– 133.

Brooks,D.R.&McLennan,D.A.(

2002). The Nature of Diversity: An Evolutionary Voyage

of Discovery. The University of Chicago Press, Chicago.

Brown,D.M.,Brenneman,R.A.,Koepﬂi,K.P.,Pollinger,J.P.,Míla,B.,

Georgiadis,N.J.,Louis,E.E.Jr.,Grether, G. F., Jacobs,D.K.&Wayne,R.

K. (2007). Extensive population genetic structure in the giraffe. BMC Biology 5, 57.

Butynski,T.M.,de Jong,Y.A.&Hearn,G.W.(

2009). Body measurements for

the monkeys of Bioko Island, Equatorial Guinea. Primate Conservation 24, 99– 105.

Camerano,L.(

1916). I caratteri del cranio, della colorazione e delle corna nella

distinzione dei camosci in specie e sottospecie. Rivista di Antropologia (Rome) 20, 3– 14.

Castley,J.G.,Boshoff,A.F.&Kerley,G.I.H.(

2001). Compromising South

Africa’s natural biodiversity – inappropriate herbivore introductions. South Africa

Journal of Science 97, 344–348.

Caughley,G.(

1994). Directions in conservation biology. Journal of Animal Ecology 63,

215– 244.

Cernohorska,H.,Kubickova,S.,Vahala,J.,Robinson,T.J.&Rubes,J.(

2011).

Cytotypes of Kirk’s dik-dik (Madoqua kirkii, Bovidae) show multiple tandem fusions.

Cytogenetics and Genome Research 132, 255– 263.

Champagnon,J.,Elmberg,J.,Guillemain,M.,Gauthier-Clerc,M.&

Lebreton,J.-D.(

2012). Conspeciﬁcs can be aliens too: a review of effects of

restocking practices in vertebrates. Journal for Nature Conservation 20, 231– 241.

Collen,B.,Turvey,S.T.,Waterman,C.,Meredith,H.M.R.,Kuhn,T.

S., Baillie,J.E.M.&Isaac,N.J.B.(

2011). Investing in evolutionary history:

implementing a phylogenetic approach for mammal conservation. Philosophical

Transactions of the Royal Society B 366, 2611 –2622.

Corbet,G.B.(

1969). The taxonomic status of the pygmy hippopotamus, Choeropsis

liberiensis, from the Niger delta. Journal of Zoology 158, 387 –394.

Corbet,G.B.(

1997). The species in mammals. In Species: The Units of Biodiversity (eds

M. F. Claridge,H.A.Dawah andM.R.Wilson), pp. 341 –356. Chapman &

Hall, London.

Corbet,G.B.&Hill,J.E.(

1986). A World List of Mammalian Species. Second Edition.

British Museum (Natural History), London.

Cordingley,J.E.,Sundaresan,S.R.,Fischhoff,I.R.,Shapiro,B.,Ruskey,

J. & Rubenstein,D.I.(

2009). Is the endangered Grevy’s zebra threatened by

hybridization? Animal Conservation 12, 505– 513.

Cotterill,F.P.D.(

2000). Reduncine antelope of the Zambezi basin. In Biodiversity

of the Zambezi Basin Wetlands (ed. J. R. Timberlake), pp. 145–199. Biodiversity

Foundation for Africa and The Zambezi Society, Bulawayo, Zimbabwe.

Cotterill,F.P.D.(

2003a). A biogeographic review of tsessebe antelopes Damaliscus

lunatus (Bovidae Alcelaphinae) in south-central Africa. Durban Musuem Novitates 28,

45–55.

Cotterill,F.P.D.(

2003b). Species concepts and the real diversity of antelopes. In

Proceedings of the Ecology and Conservation of Mini-antelope: An International Symposium on

Duiker and Dwarf Antelope in Africa (ed. A. Plowman), pp. 59– 118. Filander Verlag,

F¨urth.

Cotterill,F.P.D.(

2005).TheUpembalechweKobus anselli : an antelope new to

science emphasizes the conservation importance of Katanga, Democratic Republic

of Congo. Journal of Zoology 265, 113– 132.

Cotterill,F.P.D.(

2016). The tentelic thesis, interdisciplinarity, and earth system

science: how natural history collections underpin geobiology. Archives of Zoological

Museum of Lomonosov Moscow State University 54, 598– 635.

Cotterill,F.P.D.&Foissner,W.(

2010). A pervasive denigration of Natural

History misconstrues how biodiversity inventories and taxonomy underpin scientiﬁc

knowledge. Biodiversity Conservation 19, 291– 303.

Cotterill,F.P.D.,Taylor,P.J.,Gippoliti,S.,Bishop,J.M.&Groves,C.P.

(2014). Why one century of phenetics is enough: response to ‘‘Are there really twice

as many bovid species as we thought?’’. Systematic Biology 63, 819– 832.

Cousins,J.A.,Sadler,J.P.&Evans,J.(

2010). The challenge of regulating private

wildlife ranches for conservation in South Africa. Ecology and Society 15, 28.

Crandall,K.A.,Bininda-Emonds,O.R.P.,Mace,G.M.&Wayne,R.K.

(2000). Considering evolutionary processes in conservation biology. Trends in Ecology

& Evolution 15, 290– 295.

Cuneo,F.(

1965). Observations on the breeding of the klipspringer antelope, Oreotragus

oreotragus, and the behavior of their young born at the Naples Zoo. International Zoo

Yearbook 5, 45– 47.

D’Amen,M.,Zimmermann,N.E.&Pearman,P.B.(

2013). Conservation of

phylogeographic lineages under climate change. Global Ecology and Biogeography 22,

93– 104.

Dathe,H.(

1978). The meaning and value of breeds representing pure subspecies in

zoological gardens. Der Zoologische Garten NF 48, 164– 166.

D’Huart,J.-P.&Grubb,P.(

2001). Distribution of the common warthog (Phacochoerus

africanus) and the desert warthog (Phacochoerus aethiopicus) in the Horn of Africa. African

Journal of Ecology 39, 156– 169.

Dobzhansky,T.(

1937). Genetics and the Origin of Species. Columbia University Press,

New York.

Dubois,A.(

2003). The relationships between taxonomy and conservation biology in

the century of extinctions. Compte Rendues Biologies 326, S9–S21.

Ekblom,R.&Galindo,J.(

2011). Applications of next generation sequencing in

molecular ecology of non-model organisms. Heredity 107, 1– 15.

Ellerman,J.R.&Morrison-Scott,T.C.S.(

1951). Checklist of Palaearctic and Indian

Mammals 1758 to 1946. British Museum (Natural History), London.

Ellerman,J.R.,Morrison-Scott,T.C.S.&Hayman,R.W.(

1953). Southern

African Mammals. British Museum (Natural History), London.

Erwin,T.L.(

1991). An evolutionary basis for conservation strategy. Science 253,

750– 752.

Fagotto,F.(

1980). The caffer buffalo and its habitat in Somalia. Atti della Societ`a

Toscana Scienze Naturali Memorie B 87, 161 –179.

Fitzpatrick,B.M.,Ryan,M.E.,Johnson,J.R.,Corush,J.&Carter,E.T.

(2015). Hybridization and the species problem in conservation. Current Zoology 61,

206– 216.

Fortey,R.(

2008). Dry Storeroom. No. 1. The Secret Life of the Natural History Museum.

Random House, London.

Frade,F.(

1931). Sur l’existence en Afrique de deux especes d’elephants. Bulletin de la

Soci´et´e Portugaise des Sciences Naturelles 11, 135– 138.

Frankham,R.,Ballou,J.D.&Briscoe,D.A.(

2002). Introduction to Conservation

Genetics. Cambridge University Press, Cambridge.

Frankham,R.,Ballou,J.D.,Dudash,M.R.,Eldridge,M.D.B.,Fenster,

C. B., Lacy,R.C.,Mendelson, J. R. III, Porton,I.J.,Ralls,K.&Ryder,

O. A. (2012). Implications of different species concepts for conserving biodiversity.

Biological Conservation 153, 25– 31.

Fusari,A.&Carpaneto,G.M.(

2006). Subsistence hunting and conservation issues

in the game reserve of Gile, Mozambique. In Human Exploitation and Biodiversity

Conservation (eds D. L. Hawksworth andA.T.Bull), pp. 137 – 155. Springer,

Netherlands.

Geist,V.,O’Gara,B.&Hoffmann,R.(

2000). Taxonomy and the conservation

of biodiversity. In Ecology and Management of Large Mammals in North America (eds S.

Desmarais and P. R. Krausmann), pp. 1– 26. Prentice Hall, Upper Saddle River.

Gill,F.(

1997). Local cytonuclear extinction of the golden-winged warbler. Evolution

51, 519– 525.

Gippoliti,S.(

2010). Theropithecus gelada distribution and variations related to

taxonomy: history, challenges and conservation implications. Primates 51,291–297.

Gippoliti,S.(

2014). The forgotten donkey’s history. Remarks on African wild asses

of the Giardino Zoologico in Rome and their relevance for Equus africanus (von

Heuglin & Fitzinger, 1866) taxonomy and conservation. Der Zoologische Garten NF 83,

146– 154.

Gippoliti,S.(

2016). Questioning current practice in brown bear Ursus arctos

conservation in Europe that undervalues taxonomy. Animal Biodiversity and Conservation

39, 199– 205.

Gippoliti,S.&Amori,G.(

2007). The problem of subspecies and biased taxonomy

in conservation lists: the case of mammals. Folia Zoologica 56, 113– 117.

Gippoliti,S.,Amori,G.,Castiglia,R.,Colangelo,P.&Capanna,E.(

2014).

The relevance of Italian museum collections for research and conservation: the case

of mammals. Rendiconti Scienze Fisiche Accademia Lincei 25, 351 –357.

14 S. Gippoliti and others

Gippoliti,S.,Cotterill,F.P.D.&Groves,C.P.(2013). Mammal taxonomy

without taxonomists: a reply to Zachos and Lovari. Hystrix Italian Journal of Mammalogy

24, 145– 147.

Gippoliti,S.&Groves,C.P.(

2012). ‘‘Taxonomic inﬂation’’ in the historical context

of mammalogy and conservation. Hystrix Italian Journal of Mammalogy 23,6–9.

Goossens,B.,Salgado-Lynn,M.,Rovie-Ryan,J.J.,Ahmad,A.H.,Payne,J.,

Zainuddin,Z.Z.,Nathan,S.K.S.S.&Ambu,L.N.(

2013). Genetics and the

last stand of the Sumatran rhinoceros Dicerorhinus sumatrensis.Oryx 47, 340 –344.

Grande-Vega,M.,Farf ´

an,M.A.,Ondo,A.&Fa,J.E.(

2016). Decline in hunter

offtake of blue duikers in Bioko Island, Equatorial Guinea. African Journal of Ecology

54, 49–58.

Green,R.E.,Krause,J.,Briggs,A.W.,Maricic,T.,Stenzel,U.,Kircher,M.,

Patterson,N.,Li,H.,Zhai,W.,Fritz,M.H.Y.,Hansen, N. F., Durand,E.

Y., Malaspinas,A.S.,Jensen,J.D.,Marques-Bonet, T., et al. (2010). A draft

sequence of the Neanderthal genome. Science 328, 710– 722.

Green,W.C.H.&Rothstein,A.(

1998). Translocation, hybridization, and the

endangered black-faced impala. Conservation Biology 12, 475– 480.

Grobler,J.P.,Rushworth,I.,Brink,J.S.,Kotze,A.,Bloomer,P.,Reilly,B.

&Vrahimis,S.(

2011). Management of hybridization in an endangered endemic

species: decision making in the face of imperfect information in the case of the black

wildebeest – Connochaetes gnou.European Journal of Wildlife Research 57, 997– 1006.

Groves,C.P.(

2001). Primate Taxonomy. Smithsonian Institution, Washington.

Groves,C.P.,Fernando,P.&Robovsk ´

y,J.(

2010). The sixth rhino: a taxonomic

re-assessment of the critically endangered northern white rhinoceros. PLoS ONE

5(4), e9703.

Groves,C.P.&Grubb,P.(

2011). Ungulate Taxonomy. The Johns Hopkins University

Press, Baltimore.

Groves,C.P.&Leslie,D.M.Jr.(

2011). Family Bovidae. In Handbook of the Mammals

of the World (Volume 2, eds D. E. Wilson and R. A. Mittermeier), pp. 444 –779.

Lynx Ediciones, Barcelona.

Groves,C.P.&Smeenk,C.(

2007). The nomenclature of the African wild ass.

Zoologische Mededelingen 81, 121– 135.

Groves,C.P.,Wasser,S.K.,Roca,A.L.&Dudley,J.P.(

2016). Two African

elephant species, not just one. Nature 538, 317. (https://doi.org/10.1038/538317a).

Grubb,P.(

1993). Artiodactyla. In Mammal Species of the World. A Taxonomic and Geographic

Reference. Second Edition (eds D. E. Wilson andD.M.Reeder), pp. 377– 414.

Smithsonian Institution, Washington.

Grubb,P.(

2005). Artiodactyla. In Mammal Species of the World. A Taxonomic and

Geographic Reference. Third Edition (eds D. E. Wilson and D. M. Reeder), pp.

637– 722 Smithsonian Institution, Washington, The Johns Hopkins University

Press, Baltimore.

Grubb,P.,Groves,C.P.,Dudley,J.P.&Shoshani,J.(

2000). Living African

elephants belong to two species: Loxodonta africana (Blumenbach, 1797) and Loxodonta

cyclotis (Matschie, 1900). Elephant 2,1–4.

Guschanski,K.,Krause,J.,Sawyer,S.,Valente,L.M.,Bailey,S.,

Finstermeier,K.,Sabin,R.,Gilissen,E.,Sonet,G.,Nagy,Z.T.,Lenglet,

G., Frieder Mayer,F.&Savolainen,V.(

2013). Next-generation museomics

disentangles one of the largest primate radiations. Systematic Biology 62, 539– 554.

Haig,S.M.,Beever,E.,Chambers,S.M.,Draheim,H.M.,Dugger,B.D.,

Dunham,S.,Elliott-Smith,E.,Fontaine,J.B.,Kesler,D.C.,Knaus,

B. J., Lopes, I. F., Loschl,P.,Mullins,T.D.&Shefﬁeld,L.M.(

2006).

Taxonomic considerations in listing subspecies under the U.S. Endangered Species

Act. Conservation Biology 20, 1584– 1594.

Handley,C.O.Jr.(

1954). Book review. Southern African mammals 1758 to 1951: a

reclassiﬁcation. Journal of Mammalogy 35, 460– 461.

Harley,E.H.,de Waal,M.,Murray,S.&O’Ryan,C.(

2016). Comparison of

whole mitochondrial genome sequences of northern and southern white rhinoceroses

(Ceratotherium simum): the conservation consequences of species deﬁnition. Conservation

Genetics 17, 1285– 1291. (https://doi.org/10.1007/s10592-016-0861- 2).

Heckel, J. O., Wilhelmi, F., Kaariye,H.Y.&Gebeyehu,G.(

2008). Preliminary

Status Assessment Survey of the Critically Endangered Tora hartebeest (Alcelaphus buselaphus tora)

and Further Wild Ungulates in North-western Ethiopia. IUCN/SSC Antelope Specialist

Group Gland, Switzerland.

Heller,R.,Frandsen,P.,Lorenzen,E.D.&Siegismund,H.R.(

2013). Are there

really twice as many bovid species as we thought? Systematic Biology 62, 490– 493.

Heller,R.,Frandsen,P.,Lorenzen,E.D.&Siegismund,H.R.(

2014). Is

diagnosability an indicator of speciation? Systematic Biology 63, 833– 837.

Heller,R.,Okello,S.B.A.&Siegismund,H.(

2010). Can small wildlife

conservancies maintain genetically stable populations of large mammals? Evidence

for increased genetic drift in geographically restricted populations of Cape buffalo

in East Africa. Molecular Ecology 19, 1324– 1334.

Hoagland,K.E.(

1996). The taxonomic impediment and the convention on

biodiversity. ASC News 24(61–62), 66 –67.

Huxley, T. (ed.) (1940). The New Systematics. Oxford University Press, Oxford.

Isaac,N.J.B.,Mallet,J.&Mace,G.M.(

2004). Taxonomic inﬂation: its inﬂuence

on macroecology and conservation. Trends Ecology & Evolution 19, 464– 469.

Kimura,B.,Marshall,F.B.,Chen,S.,Rosenbom,S.,Moehlman,P.D.,

Tuross,N.,Sabin,R.C.,Peters,J.,Barbara Barich,B.,Yohannes,H.,

Kebede, F., Teclai,R.,Albano Beja-Pereira,A.&Mulligan,C.J.(

2010).

Ancient DNA from Nubian and Somali wild ass provides insights into donkey

ancestry and domestication. Proceedings of the Royal Society B 278, 50 –57.

King,I.(

2009). The need for the incorporation of phylogeny in the measurement

of biological diversity, with special reference to ecosystem functioning research.

BioEssays 31, 107– 116.

Kingswood,S.C.,Kumamoto,A.T.,Charter,S.J.&Jones,M.L.(

1998).

Cryptic chromosomal variation in suni Neotragus moschatus (Artiodactyla, Bovidae).

Animal Conservation 1, 95– 100.

Kumamoto,A.T.,Charter,S.J.,Kingswood,S.C.,Ryder,O.A.&Gallagher,

D. S. (1999). Centric fusion differences among Oryx dammah,O. gazella,andO. leucoryx

(Artiodactyla Bovidae). Cytogenetics and Cell Genetics 86, 74–80.

Kumamoto,A.T.,Kingswood,S.C.&Hugo,W.(

1994). Chromosomal divergence

in allopatric populations of Kirk’s dik dik, Madoqua kirki (Artiodactyla, Bovidae).

Journal of Mammalogy 75, 357– 364.

Larsen,P.A.,March´

an-Rivadeneira,M.R.&Baker,R.J.(

2010). Natural

hybridization generates mammalian lineage with species characteristics. Proceedings

of the National Academy of Sciences of the United States of America 107, 11447–11452.

Linder,P.H.,de Klerk,H.M.,Bor,J.,Burgess,N.D.,Fjelds ˚

a,J.&Rahbek,

C. (2012). The partitioning of Africa: statistically deﬁned biogeographical regions in

sub-Saharan Africa. Journal of Biogeography 39, 1189– 1205.

Lindsey,P.J.,Roulet,P.A.&Romanach,S.S.(

2007). Economic and

conservation signiﬁcance of the trophy hunting industry in sub-saharan Africa.

Biological Conservation 134, 455– 469.

Lorenzen,E.D.,Heller,R.&Siegismund,H.R.(

2012). Comparative

phylogeography of African savannah ungulates. Molecular Ecology 21, 3656– 3670.

Lydekker,R.(

1913). Catalogue of the Ungulate Mammals in the British Museum (Natural

History) (Volume I). British Museum (Natural History), London.

Lydekker,R.&Blaine,G.(

1913–1916). Catalogue of the Ungulate Mammals in the British

Museum (Natural History) (Volume I–IV). British Museum (Natural History), London.

Maisels, F., Strindberg,S.,Blake,S.,Wittemyer,G.,Hart,J.,Williamson,

E. A., Aba’a,R.,Abitsi,G.,Ambahe,R.D.,Amsini,F.&Bakabana,P.C.

(2013). Devastating decline of forest elephants in Central Africa. PLoS ONE 8,

e59469.

Mallet,J.(

2004). Perspectives. Poulton, Wallace and Jordan: how discoveries in Papilio

butterﬂies led to a new species concept 100 years ago. Systematics and Biodiversity 1,

441– 452.

Mallet,J.(

2005). Hybridization as an invasion of the genome. Trends in Ecology &

Evolution 20, 229– 237.

Mallet,J.(

2008). Hybridization, ecological races and the nature of species: empirical

evidence for the ease of speciation. Philosophical Transactions of the Royal Society B 363,

2971– 2986.

Marshall,T.C.&Spalton,J.A.(

2000). Simultaneous inbreeding and outbreeding

depression in reintroduced Arabian oryx. Animal Conservation 3, 241– 248.

Matthee,C.A.&Robinson,T.J.(

1999). Cytochrome bphylogeny of the family

Bovidae: resolution within Alcelaphini, Antilopini, Neotragini and Tragelaphini.

Molecular Phylogenetics and Evolution 12,31–46.

Mayr,E.(

1942). Systematics and the Origin of Species from the Viewpoint of a Zoologist.

Columbia University Press, New York.

McDevitt,A.D.,Mariani,S.,Hebblewhite,M.,Decesare,N.J.,Morgantini,

L., Seip,D.,Weckworth,B.V.&Musiani,M.(

2009). Survival in the Rockies

of an endangered hybrid swarm from diverged caribou (Rangifer tarandus) lineages.

Molecular Ecology 18, 665– 679.

Meester,J.&Setzer,H.W.(eds)(

1971). The Mammals of Africa. An Identiﬁcation

Manual. Smithsonian Institution Press, Washington.

de Merode,E.,Homewood,K.&Cowlishaw,G.(

2004). The value of bushmeat

and other wild foods to rural households living in extreme poverty in Democratic

Republic of Congo. Biological Conservation 118, 573– 581.

Melter,D.G.A.(

1993). Historical survey of disease problems in wildlife populations:

Southern Africa mammals. Journal Zoo and Wildlife Medicine 24, 237 –244.

Moodley,Y.&Bruford,M.W.(

2007). Molecular biogeography: towards an

integrated framework for conserving Pan-African biodiversity. PLoS ONE 2, e454.

Moodley,Y.,Russo,I.-R.M.,Dalton,D.L.,Kotz ´

e,A.,Muya,S.,Haubensak,

P., B´

alint,B.,Munimanda,G.K.,Deimel,C.,Setzer,A.,Dicks,K.,

Herzig-Straschil,B.,Kalthoff,D.C.,Siegismund,H.R.,Robovsk´

J., et al. (2017). Extinctions, genetic erosion and conservation options for the black

rhinoceros (Diceros bicornis). Scientiﬁc Reports 7, 41417.

Moritz,C.(

1994). Deﬁning ‘evolutionarily signiﬁcant units’ for conservation. Trends

in Ecology & Evolution 9, 373– 375.

Morrison, W. R. III, Lohr,J.L.,Duchen,P.,Wilches,R.,Trujillo,D.,Mair,

M. & Renner,S.S.(

2009). The impact of taxonomic change on conservation: does

it kill, can it save, or is it just irrelevant? Biological Conservation 142, 3201– 3206.

Mouquet,N.,Devictor,V.,Meynard,C.N.,Munoz, F., Bersier,L.F.,Chave,

J., Couteron,P.,Dalecky,A.,Fontaine,C.,Gravel,D.,Hardy,O.J.,Jabot,

F., Lavergne,S.,Leibold,M.,Mouillot,D.,M¨

unkem¨

uller,T.,Pavoine,S.,

Prinzing,A.,Rodrigues,A.S.L.,Rohr,R.P.,Th ´

ebault,E.&Thuiller,W.

(2012). Ecophylogenetics: advances and perspectives. Biological Reviews 87, 769–785.

Taxonomic inertia and ungulate conservation 15

Nasi,R.,Taber,A.&Van Vliet,N.(2011). Empty forests, empty stomachs?

Bushmeat and livelihoods in the Congo and Amazon basin. International Forestry

Review 13, 335– 368.

Newing,H.(

2001). Bushmeat hunting and management: implications of duiker

ecology and interspeciﬁc competition. Biodiversity Conservation 10, 99– 108.

Nijhof,A.M.,Pillay,V.,Steyl,J.,Prozesky,L.,Stoltsz,W.H.,Lawrence,J.

A., Penzhorn,B.L.&Jongejan,F.(

2005). Molecular characterization of Theileria

species associated with mortality in four species of African Antelopes. Journal of

Clinical Microbiology 43, 5907– 5911.

O’Brien,S.J.,Roelke,M.E.,Marker,L.,Newman,A.,Winkler,C.A.,

Meltzer,D.,Colly,L.,Evermann, J. F., Bush,M.&Wildt,D.E.(

1985).

Genetic basis for species vulnerability in the cheetah. Science 227, 1428– 1434.

O’Hara,R.J.(

1988). Homage to Clio, or, toward an historical philosophy for

evolutionary biology. Systematic Biology 37, 142– 155.

Ouma,C.,Roca,A.L.,Were,T.,Raballah, E. O., Oguge, N. O., Jura,W.G.Z.

O., Ochieng,J.W.,Hanotte,O.&Georgiadis,N.(

2011). Genetic structure

of hartebeest populations straddling a transition zone between morphotypes. Journal

of Basic and Applied Scientiﬁc Research 1, 131– 149.

Pagacova,E.,Cernohorska,H.,Kubickova,S.,Vahala,J.&Rubes,J.(

2011).

Centric fusion polymorphism in captive animals of family Bovidae. Conservation

Genetics 12, 71– 77.

de Queiroz,K.(

1999). The general lineage concept of species and the deﬁning

properties of the species category. In Species: New Interdisciplinary Essays (ed. R. A.

Wilson), pp. 49– 89. MIT Press, Cambridge.

de Queiroz,K.(

2007). Species concepts and species delimitation. Systematic Biology

56, 879– 886.

Ralls,K.,Brugger,K.&Glick,A.(

1980). Deleterious effects of inbreeding in a

herd of captive dorcas gazelle Gazella dorcas.International Zoo Yearbook 20, 137 –146.

Reddy,S.&D´

avolos,L.M.(

2003). Geographical sampling bias and its implications

for conservation priorities in Africa. Journal of Biogeography 30, 1719– 1727.

Rhymer,J.M.&Simberloff,D.(

1996). Extinction by hybridization and

introgression. Annual Review of Ecology and Systematics 27, 83–109.

Richards,Z.T.&Hobbs,J.P.A.(

2015). Hybridisation on coral reefs and the

conservation of evolutionary novelty. Current Zoology 61, 132– 145.

Robinson,T.J.,Cernohorska,T.,Diedericks,G.,Cabelova,K.,Duran,A.

&Matthee,C.A.(

2014). Phylogeny and vicariant speciation of the Grey Rhebok,

Pelea capreolus.Heredity 112, 325–332.

Robinson,T.J.,Cernohorska,H.,Schulze,E.&Duran-Puig,A.(

2015).

Molecular cytogenetics of tragelaphine and alcelaphine interspecies hybrids:

hybridization, introgression and speciation in some African antelope. Biological

Letters 11, 20150707 (https://doi.org/10.1098/rsbl.2015.0707).

Robinson,T.J.&Ropiquet,A.(

2011). Examination of hemiplasy, homoplasy and

phylogenetic discordance in chromosomal evolution of the Bovidae. Systematic Biology

60, 439– 450.

Roca,A.L.,Ishida,Y.,Brandt,A.L.,Benjamin,N.R.,Zhao,K.&Georgiadis,

N. J. (2015). Elephant natural history: a genomic perspective. Annual Review of Animal

Biosciences 3, 139– 167.

Rodríguez, F., Hammer,S.,P´

erez,T.,Suchentrunk, F., Lorenzini,R.,

Michallet,J.,Martinkova,N.,Albornoz,J.&Domínguez,A.(

2009).

Cytochrome bphylogeography of chamois (Rupicapra spp.). Population contractions,

expansions and hybridizations governed the diversiﬁcation of the genus. Journal of

Heredity 100, 47– 55.

Rohland,N.,Reich,D.,Mallick,S.,Meyer,M.,Green,R.E.,Georgiadis,N.

J., Roca,A.L.&Hofreiter,M.(

2010). Genomic DNA sequences from mastodon

and woolly mammoth reveal deep speciation of forest and savanna elephants. PLoS

Biology 8, e1000564.

Rookmaaker,K.(

2000). The alleged population reduction of the southern white

rhinoceros (Ceratotherium simum simum) and the successful recovery. S¨augetierkundliche

Mitteilungen 45, 55– 70.

Roos,C.,Zinner,D.,Kubatko,L.S.,Schwarz,C.,Yang,M.,Meyer,D.,Nash,

S. D., Xing,J.,Batzer,M.A.,Brameier,M.,Leendertz,F.H.,Ziegler,

T., Perwitasari-Farajallah,D.,Nadler,T.,Walter,L.&Osterholz,M.

(2011). Nuclear versus mitochondrial DNA: evidence for hybridization in colobine

monkeys. BMC Evolutionary Biology 11,77.

Rothschild,W.(

1921). On two new races of Oryx.Annals and Magazine of Natural

History 8,209–210.

Rothschild,W.,Hartert,E.&Jordan,K.(

1903). Note of the editors. Novitates

Zoologicae 1,1.

Rowe,K.C.,Singhal,S.,Macmanes,M.D.,Ayroles, J. F., Morelli,T.L.,

Rubidge,E.M.,Bi,K.E.&Moritz,C.C.(

2011). Museum genomics: low-cost

and high-accuracy genetic data from historical specimens. Molecular Ecology Resources

11, 1082– 1092.

Ruxton,A.E.&Schwarz,E.(

1929). On hybrid hartebeests and on the distribution

of the Alcelaphus buselaphus group. Proceedings of the Zoological Society of London 99,

567– 583.

Ryder,O.A.(

1986). Species conservation and systematic: the dilemma of subspecies.

Trends Ecology & Evolution 1, 9– 10.

Rylands,A.B.&Mittermeier,R.A.(

2014). Primate taxonomy: species and

conservation. Evolutionary Anthropology 23, 8– 10.

Sarasa,M.(

2013). Trophy hunting, size, rarity and willingness to pay: inter-speciﬁc

analysis of trophy prices require reliable speciﬁc data. Animal Biodiversity and

Conservation 36, 165– 175.

Schwarz,E.(

1914). Notes on African ungulates. I. The classiﬁcation of the duikers.

Annals and Magazine of Natural History 13, 491– 495.

Schwenk,K.,Brede,N.&Streit,B.(

2008). Introduction. Extent, processes and

evolutionary impact of interspeciﬁc hybridization in animals. Philosophical Transactions

of the Royal Society B 363, 2805 –2811.

Sclater,P.L.&Thomas,O.(

1894–1900). The Book of Antelopes (Volume 4). R.H.

Porter, London.

Shetty,N.R.&Vidya,T.N.C.(

2011). To split or not to split: the case of the

African elephant. Current Science 100, 810–812.

Simberloff,D.(

1996). Hybridization between native and introduced wildlife species:

importance for conservation. Wildlife Biology 2, 143– 150.

Spear,D.&Chown,S.L.(

2009). The extent and impacts of ungulate translocations:

South Africa in a global context. Biological Conservation 142, 353– 363.

Stanton,D.W.G.,Hart,J.,Galbusera,P.,Helsen,P.,Shephard,J.,K¨

umpel,

N. F., Wang,J.,Ewen,J.G.&Bruford,M.W.(

2014). Distinct and diverse:

range-wide phylogeography reveals ancient lineages and high genetic variation in

the endangered okapi (Okapia johnstoni). PLoS ONE 9, e101081.

Starin,E.D.(

2000). Notes on the sitatunga in The Gambia. African Journal of Ecology

38, 339– 342.

Steiner,C.C.,Charter,S.J.,Goddard,N.,Davis,H.,Brandt,M.,Houck,

M. L. & Ryder,O.A.(

2016). Chromosomal variation and perinatal mortality in

San Diego Zoo Soemmerring’s gazelles. Zoo Biology 34, 374– 384.

Storfer,A.(

1999). Gene ﬂow and endangered species translocation: a topic revised.

Biological Conservation 87, 173– 180.

Templeton,A.R.(

1986). Coadaptation and breeding depression. In Conservation

Biology: The Science of Scarcity and Diversity (ed. M. E. Soul´

e), pp. 105– 116. Sinauer

Associates, Sunderland.

Templeton,A.R.&Read,A.B.(

1998). Elimination of inbreeding depression from

a captive population of Speke’s gazelle: validity of the original statistical analysis and

conﬁrmation by permutation testing. Zoo Biology 17, 77– 98.

Themudo,G.E.,Ruﬁno,A.C.&Campos,P.F.(

2015). Complete mitochondrial

DNA sequence of the endangered giant sable antelope (Hippotragus niger variani):

insights into conservation and taxonomy. Molecular Phylogenetics and Evolution 83,

242– 249.

Thomas,O.(

1902). On the East-African representative of the bongo and its generic

position. Annals and Magazine of Natural History 10, 309– 310.

Thomassen,H.A.,Freedman,A.H.,Brown,D.M.,Buermann,W.&Jacob,D.

K. (2013). Regional differences in seasonal timing of rainfall discriminate between

genetically distinct East African giraffe taxa. PLoS ONE 8, e77191.

Turvey,S.T.(

2009). Holocene mammal extinctions. In Holocene Extinctions (ed. S. T.

Turvey), pp. 41– 61. Oxford University Press, Oxford.

Van Aswegen,E.,Labuschagne,C.&Grobler,J.P.(

2012). Phenotypic

differences, spatial distribution and diversity at the CYTb and BMP4 genes in

springbok (Antidorcas marsupialis). Mammalian Biology 77, 391–396.

Vane-Wright,R.I.,Humphries,C.J.&Williams,P.H.(

1991). What to protect?

Systematics and the agony of choice. Biological Conservation 55, 235– 254.

Verkaar,E.L.C.,Nijman,I.J.,Beeke,M.,Hanekamp,E.&Lenstra,J.A.

(2004). Maternal and paternal lineages in cross-breeding Bovine species. Has wisent

a hybrid origin? Molecular Biology and Evolution 21, 1165– 1170.

van der Walt,J.,Nel,L.H.&Hoelzel,A.R.(

2013). Differentiation at

mitochondrial and nuclear loci between the blesbok (Damaliscus pygargus phillipsi)

and bontebok (D. p. pygargus): implications for conservation strategy. Conservation

Genetics 14, 243– 248.

Wandeler,P.,Hoeck,P.E.A.&Keller,L.F.(

2007). Back to the future: museum

specimens in population genetics. Trends Ecology and Evolution 22, 634– 642.

Wilting,A.,Courtiol,A.,Christiansen,P.,Niedballa,J.,Scharf,A.K.,

Orlando,L.,Balkenhol,N.,Hofer,H.,Kramer-Schadt,S.,Fickel,J.

&Kitchener,A.C.(

2015). Planning tiger recovery: understanding intraspeciﬁc

variation for effective conservation. Science Advances 1, e1400175 (https://doi.org/10

.1126/sciadv.1400175).

van Wyk,A.M.,Dalton,D.L.,Hoban,S.,Bruford,M.W.,Russo,I.-R.M.,

Birss,C.,Grobler,P.,van Vuuren,B.J.&Kotz´

e,A.(

2017). Quantitative

evaluation of hybridization and the impact on biodiversity conservation. Ecology and

Evolution 7, 320– 330.

Yasuoka,H.(

2006). The sustainability of duikers (Cephalophus spp.) hunting for the Baka

hunter-gatherers in south-eastern Cameroon. African Studies Monograph Supplement 33,

95– 120.

Zachos,F.E.,Apollonio,M.,B¨

armann,E.V.,Festa-Bianchet,M.,G¨

ohlich,

U., Habel,J.C.,Haringa,E.,Kruckenhausera,L.,Lovari,S.,McDevitth,

A. D., Pertoldi,C.,R¨

ossner,G.C.,Sanchez-Villagra,M.R.,Scandura,

M. & Suchentrunk,F.(

2013a). Species inﬂation and taxonomic artefacts – A

critical comment on recent trends in mammalian classiﬁcation. Mammalian Biology

78,1–6.

16 S. Gippoliti and others

Zachos,F.E.,Clutton-Brock,T.H.,Festa-Bianchet,M.,Lovari,S.,

Macdonald,D.W.&Schaller,G.B.(

2013b). Taxonomy: species splitting

puts conservation at risk. Nature 494, 35.

Zinner,D.,Arnold,M.L.&Roos,C.(

2009). Is the new primate genus Rungwecebus

a baboon? PLoS ONE 4, e4859.

Zinner,D.,Arnold,M.L.&Roos,C.(

2011). The strange blood: natural

hybridization in primates. Evolutionary Anthropology 20, 96– 103.

Zschokke,S.,Armbruster,G.F.J.,Ursenbacher,S.&Bauer,B.

(2011). Genetic differences between the two remaining wild populations of

the endangered Indian rhinoceros (Rhinoceros unicornis). Biological Conservation 144,

2702– 2709.

Zschokke,S.&Baur,B.(

2002). Inbreeding, outbreeding, infant growth, and size

dimorphism in captive Indian rhinoceros (Rhinoceros unicornis). Canadian Journal of

Zoology 80, 2014– 2023.

(Received 1 July 2016; revised 23 March 2017; accepted 27 March 2017 )

Genomics of historical museum collections clarifies species diversity in Cuban hutias (Capromys)

Article

Oct 2024
J MAMMAL

Specimen-based taxonomic research is essential for understanding diversity and setting management frameworks for threatened mammal faunas, and ancient DNA techniques are increasingly used to extract information from taxonomically relevant historical specimens. The largest survivors of the depleted Caribbean mammal fauna are hutias in the genus Capromys, which is usually interpreted as containing a single species, C. pilorides. Previous studies have demonstrated genetic differentiation of Capromys populations across Cuba, but infrageneric species diversity and nomenclature remain unclear. We conducted ancient DNA analysis of historical Capromys samples using cytochrome b and complete mitogenome data sets, and including the 19th-century holotypes of 2 species now considered synonyms, C. fournieri and C. geayi. Our analyses identify distinct western and central/eastern Capromys clades that diverged 1.75 Mya based upon mitogenome data. These clades are separated by the Havana–Matanzas Channel, which represented a barrier to dispersal throughout the Neogene–Quaternary. Divergence date comparisons with other hutia species provide support for interpreting divergence between Capromys populations as species-level differentiation. Although we were unable to yield amplifiable DNA from the C. fournieri holotype, our analyses confidently assign the C. geayi holotype to the western Capromys clade. We therefore recognize 2 extant Capromys species: C. geayi (western Cuba) and C. pilorides (central/eastern Cuba and Cayman Islands).

Lost species, neglected taxonomy, and the role of natural history collections and synonymization in the identification of the World’s forgotten biodiversity

Article

Full-text available

Oct 2024

A recent paper highlighted the need for increased attention towards species that have vanished from scientific literature and proposed a new nomenclature in view of needed conservation actions, based on the time interval since their disappearance. Here, we propose to implement this concept by showcasing a taxonomic perspective that is often overlooked in conservation studies. In recent decades, research on vertebrates showed that, in several cases, species considered as undescribed were, in fact, first discovered and already named a long time ago. Quite often they fell into oblivion while being considered synonyms of other taxa until they were re-evaluated in subsequent taxonomic revisions. In this context, we are proposing the concept of “long-lost synonymized” species, asking for greater attention to the discipline of taxonomy, the relevance of specimen-based taxonomy and the value of natural history collections within conservation and academic communities.

The 5 'D'S of taxonomy: A user's guide

Article

Aug 2024
Q REV BIOL

Colin Favret

Much of what has recently been written about taxonomy has focused on negatives in the face of a heterogeneously defined taxonomic impediment. The current review takes a step back from the rhetoric to explicate the modern science of taxonomy with a new practical model, "the five 'D's": taxon discovery, delimitation, diagnosis, description, and specimen determination. Although individual taxonomists may focus more on some of these practices and less on others, taxonomy as a discipline requires all five. Each practice depends on the one prior and necessarily leads to and often overlaps with the one following. In fact, the first 'D'-taxon discovery-has its origin in the last, specimen determination, thereby closing a recursive loop of taxonomic progress. Hopefully users of taxonomy-almost all biologists-will appreciate a fresh perspective on a foundational science. Several recommendations are offered to biological researchers to account for the iterative improvement, and hence necessary change, in the taxonomy and nomenclature of their study organisms.

Taxonomy and systematics of the Neotropical primates: a review and update

Article

Full-text available

May 2024

The database of the IUCN SSC Primate Specialist Group currently (December 2023) registers 218 species and subspecies of Neotropical primates in 24 genera and five families. In the early 1960s, the diversity of Neotropical primates was estimated to be around 200 species and subspecies. From then, through the 1970s to the mid-1990s, however, the perception of the region’s primate diversity dropped, and reached an all-time low at 83 species and subspecies in 1980 (A World List of Mammalian Species, G. B. Corbet and J. E. Hill, British Museum (Natural History), Comstock Publishing, Cornell University Press, London and Ithaca). Interest in taxonomy and primate field research in the Neotropics was subdued up to the late 1970s. Change was sparked by the burgeoning capture of primates for biomedical research in the 1950s and 1960s, and the increasing destruction of the Amazon rainforests from the late 1970s. The numbers increased, at first slowly, but then, in 1995, they leapt back to the 200s in anticipation of a book by C. P. Groves (2001, Primate Taxonomy, Smithsonian Institution Press, Washington, DC). The species’ counts (not including subspecies) rose due to the adoption of the Phylogenetic Species Concept over the Biological Species Concept, the former favoring the category of species over subspecies. In this article, we discuss the changes in species and subspecies numbers in the classification of the Neotropical primates, and report on the taxonomic changes resulting from taxonomic research ongoing since 2012. We emphasize the importance of taxonomic research for an understanding of the diversity of primates, and for conservation planning, not least in identifying the populations that are threatened.

Taxonomy, Distribution, and Conservation of Prigogine's Angola Colobus Colobus angolensis prigoginei Verheyen, 1959 (Primates: Cercopithecidae)

Article

Full-text available

Apr 2024

Conservation genetics of Sclerocactus in Colorado: the importance of accurate taxonomy to conservation

Article

Full-text available

Dec 2023

Introduction Recent advances in genetic data collection utilizing next-generation DNA sequencing technologies have the potential to greatly aid the taxonomic assessment of species of conservation concern, particularly species that have been difficult to describe using morphology alone. Accurate taxonomic descriptions aided by genetic data are essential to directing limited conservation resources to species most in need. Sclerocactus glaucus is a plant endemic to Western Colorado that is currently listed as Threatened under the Endangered Species Act (ESA). However, in 2023, the U. S. Fish and Wildlife Service proposed de-listing S. glaucus from the ESA due to recovery of the species. Previous research had found substantial genetic structure between populations in the northern part of the S. glaucus range relative to the majority of the species distribution. Methods In this study we utilized double-digest Restriction-site Associated DNA sequencing (RAD-seq) in order to better understand the genetic structure of S. glaucus . Results Our results indicate that S. glaucus contains two distinct evolutionary lineages that warrant recognition at the level of species, with what was previously described as S. glaucus North being recognized as Sclerocactus dawsoniae . Discussion The newly described S. dawsoniae has a limited estimated number of individuals, low levels of nucleotide diversity, a very narrow geographic range, and an uneven geographic distribution with most plants being found in a single management area, all of which supports continued direct conservation of this species. In contrast, S. glaucus has a large estimated minimum population size, a broad geographic range that includes numerous protected areas, and adequate levels of genetic diversity. Without further conservation action, a delisting decision for S. glaucus will simultaneously remove all Endangered Species Act protections for S. dawsoniae . The current work demonstrates the importance of having robust genetic datasets when planning conservation activities for species of concern. Moving forward, we recommend that government stakeholders prioritize supporting genetic studies of endangered species prior to making any changes to listing decisions.

How many species of Rafflesia exist in Java, Indonesia and what are the implications for conservation?

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Full-text available

Nov 2023

Societal Impact Statement Clarifying species status for closely related taxa with similar and overlapping morphology is important for planning conservation efforts. Conservation of Rafflesia goes beyond merely saving species from extinction. It has far‐reaching societal impacts that touch on scientific discovery, cultural heritage, economic development, education, and more. Rafflesia interests many nature lovers, and so protected areas that preserve Rafflesia can become tourism hotspots, contributing to local economies and livelihoods. By conserving biodiversity, we acknowledge and value the interdependence of all living organisms, promoting a holistic understanding of nature. Biodiversity conservation is an investment in the health and well‐being of both ecosystems and human societies. Summary Species ambiguity could hinder conservation activities. Rafflesia is an endangered, holoparasitic, and endophytic plant genus that grows exclusively on Tetrastigma (Vitaceae) host plants. Overlapping morphological characters make their species delimitation difficult. Therefore, the number of Rafflesia species has been a major debate until now. On the island of Java, Indonesia, two or three species have been variously recognized. Here, we aim to illuminate the species status using single nucleotide polymorphisms (SNPs) marker obtained via a multiplexed ISSR genotyping by sequencing (MIG‐seq) approach. Clustering analysis with STRUCTURE indicates three different groups. Furthermore, the delimitation of the Javanese Rafflesia into three species is the favored model based on SNAPPER analysis. Phylogenetic analysis using Randomized Axelerated Maximum Likelihood (RAxML) also supports the distinction of the three groups. Although a SplitsTree4 analysis confirms the abovementioned results, it also highlights that Rafflesia patma shows broader gene flow compared to the other two species R. rochusenii and R. zollingeriana . We conclude that there are likely three species of Rafflesia on Java. Our study highlights the ability of using SNPs markers, in this case derived from a MIG‐seq approach, in approaching species uncertainty. The importance of clarifying the Rafflesia species status on Java Island for conservation planning is also discussed.

Designation of a New Subspecies of Angola Colobus Colobus angolensis Sclater, 1860 (Primates: Cercopithecidae) Endemic to the Mahale Mountains of Western Tanzania

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Feb 2024

The polytypic Angola colobus Colobus angolensis is a widespread species that, in eastern Africa, is often restricted to small, highly isolated, areas. In 1966, evidence for an undescribed subspecies of C. angolensis was obtained in Mahale Mountains National Park, central west Tanzania. Mahale C. angolensis has only been observed twice by scientists (1976 and 1979) and remained unnamed. In April 2022, 43 years after the last published observation, we observed, heard, and photographed a group of Mahale C. angolensis. Given the considerable current geographic isolation (~100 km across L. Tanganyika; ~330 km across land) of this monkey from its conspecifics, together with the distinctive coloration and pattern of its pelage, we here designate this as a new subspecies. We also describe the environment in which Mahale C. angolensis lives, discuss its paleobiogeography, taxonomic arrangement, and threats, and provide recommendations for conservation and research. Mahale C. angolensis is endemic to the montane forests of Mahale Mountains National Park where it has been observed at only two sites, the south slope of Mt. Ihumo (~1,970 m asl) and on the ridge between Mt. Nkungwe and Mt. Kahoko (~2,350 m asl). In addition, bouts of 'roar' loud calls were heard on nearby Mt. Mhensabantu (~2,050 m asl) on two occasions. The geographic distribution of Mahale C. angolensis is likely between 10 km² and 50 km². The size of this population is probably <400 individuals, with <200 adults. This monkey appears to occur wholly within a remote and rugged part of Mahale Mountains National Park where agricultural encroachment and poaching are not major concerns at this time. The primary threats are habitat loss due to fire, and to a warming climate. With its small population and severely restricted geographic distribution, Mahale C. angolensis qualifies as a 'Critically Endangered' subspecies under current IUCN Red List degree of threat criteria.

Common names of the Asiatic ibex superspecies at a turning point in its taxonomy and management

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Full-text available

Feb 2023

Mathieu Sarasa

Common names of species matter in species management. However, taxonomic inertia and a blurred perception of a species can hinder the updating of framework documents and conservation schemes. Ibexes from Asia are a notable case of a polytypic species with numerous common names. This review examines data on the common names and taxonomy used for this superspecies. Some taxonomic units and common names are more consistent with recent genetic data than others and highlight management and/or conservation issues. The standardized use of this information in management schemes for the Capra sibirica complex will help lessen the risk of the extinction of distinguishable ibex conservation units from Asia, and, indirectly, of other species that share their geographical ranges.

Integrative taxonomy clarifies the evolution of a cryptic primate clade

Article

Full-text available

Sep 2024
Nat. Ecol. Evol.

Global biodiversity is under accelerating threats, and species are succumbing to extinction before being described. Madagascar’s biota represents an extreme example of this scenario, with the added complication that much of its endemic biodiversity is cryptic. Here we illustrate best practices for clarifying cryptic diversification processes by presenting an integrative framework that leverages multiple lines of evidence and taxon-informed cut-offs for species delimitation, while placing special emphasis on identifying patterns of isolation by distance. We systematically apply this framework to an entire taxonomically controversial primate clade, the mouse lemurs (genus Microcebus, family Cheirogaleidae). We demonstrate that species diversity has been overestimated primarily due to the interpretation of geographic variation as speciation, potentially biasing inference of the underlying processes of evolutionary diversification. Following a revised classification, we find that crypsis within the genus is best explained by a model of morphological stasis imposed by stabilizing selection and a neutral process of niche diversification. Finally, by clarifying species limits and defining evolutionarily significant units, we provide new conservation priorities, bridging fundamental and applied objectives in a generalizable framework.

Extinctions, genetic erosion and conservation options for the black rhinoceros (Diceros bicornis) OPEN

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Full-text available

Feb 2017

The black rhinoceros is again on the verge of extinction due to unsustainable poaching in its native range. Despite a wide historic distribution, the black rhinoceros was traditionally thought of as depauperate in genetic variation, and with very little known about its evolutionary history. This knowledge gap has hampered conservation efforts because hunting has dramatically reduced the species’ once continuous distribution, leaving five surviving gene pools of unknown genetic affinity. Here we examined the range-wide genetic structure of historic and modern populations using the largest and most geographically representative sample of black rhinoceroses ever assembled. Using both mitochondrial and nuclear datasets, we described a staggering loss of 69% of the species’ mitochondrial genetic variation, including the most ancestral lineages that are now absent from modern populations. Genetically unique populations in countries such as Nigeria, Cameroon, Chad, Eritrea, Ethiopia, Somalia, Mozambique, Malawi and Angola no longer exist. We found that the historic range of the West African subspecies (D. b. longipes), declared extinct in 2011, extends into southern Kenya, where a handful of individuals survive in the Masai Mara. We also identify conservation units that will help maintain evolutionary potential. Our results suggest a complete re-evaluation of current conservation management paradigms for the black rhinoceros.

Quantitative evaluation of hybridization and the impact on biodiversity conservation

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Full-text available

Nov 2016

Anthropogenic hybridization is an increasing conservation threat worldwide. In South Africa, recent hybridization is threatening numerous ungulate taxa. For example, the genetic integrity of the near‐threatened bontebok (Damaliscus pygargus pygargus) is threatened by hybridization with the more common blesbok (D. p. phillipsi). Identifying nonadmixed parental and admixed individuals is challenging based on the morphological traits alone; however, molecular analyses may allow for accurate detection. Once hybrids are identified, population simulation software may assist in determining the optimal conservation management strategy, although quantitative evaluation of hybrid management is rarely performed. In this study, our objectives were to describe species‐wide and localized rates of hybridization in nearly 3,000 individuals based on 12 microsatellite loci, quantify the accuracy of hybrid assignment software (STRUCTURE and NEWHYBRIDS), and determine an optimal threshold of bontebok ancestry for management purposes. According to multiple methods, we identified 2,051 bontebok, 657 hybrids, and 29 blesbok. More than two‐thirds of locations contained at least some hybrid individuals, with populations varying in the degree of introgression. HYBRIDLAB was used to simulate four generations of coexistence between bontebok and blesbok, and to optimize a threshold of ancestry, where most hybrids will be detected and removed, and the fewest nonadmixed bontebok individuals misclassified as hybrids. Overall, a threshold Q‐value (admixture coefficient) of 0.90 would remove 94% of hybrid animals, while a threshold of 0.95 would remove 98% of hybrid animals but also 8% of nonadmixed bontebok. To this end, a threshold of 0.90 was identified as optimal and has since been implemented in formal policy by a provincial nature conservation agency. Due to widespread hybridization, effective conservation plans should be established and enforced to conserve native populations that are genetically unique.

Phylogeographic Patterns in Africa and High Resolution Delineation of Genetic Clades in the Lion (Panthera leo)

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Full-text available

Aug 2016

Comparative phylogeography of African savannah mammals shows a congruent pattern in which populations in West/Central Africa are distinct from populations in East/Southern Africa. However, for the lion, all African populations are currently classified as a single subspecies (Panthera leo leo), while the only remaining population in Asia is considered to be distinct (Panthera leo persica). This distinction is disputed both by morphological and genetic data. In this study we introduce the lion as a model for African phylogeography. Analyses of mtDNA sequences reveal six supported clades and a strongly supported ancestral dichotomy with northern populations (West Africa, Central Africa, North Africa/Asia) on one branch, and southern populations (North East Africa, East/Southern Africa and South West Africa) on the other. We review taxonomies and phylogenies of other large savannah mammals, illustrating that similar clades are found in other species. The described phylogeographic pattern is considered in relation to large scale environmental changes in Africa over the past 300,000 years, attributable to climate. Refugial areas, predicted by climate envelope models, further confirm the observed pattern. We support the revision of current lion taxonomy, as recognition of a northern and a southern subspecies is more parsimonious with the evolutionary history of the lion.

Questioning current practice in brown bear, Ursus arctos, conservation in Europe that undervalues taxonomy

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Full-text available

Jul 2016

Spartaco Gippoliti

The present paper highlights problems associated with the currently-accepted taxonomy of brown bear, Ursus arctos, and their consequences for conservation at the European level. The enormous morphological variability within Ursus arctos is not acknowledged in current taxonomy and conservation practice. Seven major clades are recognized in Ursus arctos by molecular researchers, and although Western Europe maintains most of the populations belonging to the relict Clade 1 brown bear lineage, no reference to this is made in current conservation policy. Furthermore, the tiny population of Apennine brown bears, characterized by unique skull morphology, is not even recognized as a distinct ESU (evolutionari significant unit) by current European legislation, nor is it included in the IUCN Red List. This may have serious consequences as brown bear conservation in Western Europe has been mainly based on restocking and reintroduction programs.

Ungulate Taxonomy

Book

Jan 2011

Bob Surname

Phylogeography: The History and Formation of Species

Book

Jan 2000

JOHN C. AVISE

Introduction to Conservation Genetics

Book

Mar 2002

The biological diversity of our planet is being depleted due to the direct and indirect consequences of human activity. As the size of animal and plant populations decrease, loss of genetic diversity reduces their ability to adapt to changes in the environment, with inbreeding depression an inevitable consequence for many species. This textbook provides a clear and comprehensive introduction to the importance of genetic studies in conservation. The text is presented in an easy-to-follow format with main points and terms clearly highlighted. Each chapter concludes with a concise summary, which, together with worked examples and problems and answers, emphasise the key principles covered. Text boxes containing interesting case studies and other additional information enrich the content throughout, and over 100 beautiful pen and ink portraits of endangered species help bring the material to life.

LOCAL CYTONUCLEAR EXTINCTION OF THE GOLDEN-WINGED WARBLER

Article

Apr 1997
EVOLUTION

Frank B Gill

I compared the mtDNA compositions of two adjacent populations of Vermivora chrysoptera (golden-winged warbler) at different stages of transient hybridization with its sister species V. pinus (blue-winged warbler). Pinus mtDNA introgresses asymmetrically and perhaps rapidly into chrysoptera phenotypes without comparable reverse introgression of chrysoptera mtDNA into replacing pinus populations. Pinus mtDNA was virtually fixed (98%) in an actively hybridizing lowland population with varied phenotypes. Pinus mtDNA increased from 27% (n = 11) in 1988 to 70% (n = 10) in 1992 in successive samples of a highland population in the initial stages of hybridization. This population comprised mostly pure and slightly introgressed chrysoptera phenotypes. The rapid pace of asymmetrical introgression may be the result of initial invasion of chrysoptera populations by pioneering female pinus and/or an unknown competitive advantage of pinus females and their daughters over chrysoptera females.

On the East-African representatives of the bongo and its generic position

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