Species complex, cryptic species and the

need for Integrative taxonomy

K. Praveen Karanth

CES, IISc, Bangalore

National Seminar on Conservation Biotechnology and

DNA Barcoding, 18-19th May 2015

Gujarat Biodiversity Gene Bank

4Hanuman SL

Hanuman Sl

Nilgiri

Purple-faced

Phylogeny Phylogeny of of langurslangurs of the Indian subcontinentof the Indian subcontinent

Hanuman N

Silvered

Dusky

Francois'

Phayre's (V)

Phayre's (I)

Hanuman N

Karanth et al. (2005) Molecular Phylogenetics and Evolution

Spalax galili, 2n=52

is distributed predominantly

in the cool and humid Upper

Galilee Mountains

Spalax golani, 2n=54

is distributed in the cool

and semi-dry Golan

Heights

Spalax carmeli, 2n=58

is distributed in the

In Israel the 4 chromosomal (cryptic) species are distributed parapatrically in 4 climatic regimes

Spalax judaei, 2n=60

is distributed in the warm

and dry southern Coastal

Plains and northern

Negev Desert

is distributed in the

humid and warm Lower

Galilee Mountains

and central Coastal Plains

Karanth et al. 2004

Both Hanuman langur and blind mole rat are widely distributed.

Widely distributed species are often species complexes and

harbor cryptic diversity.

Species complex: Group of closely related, morphologically similar Species complex: Group of closely related, morphologically similar

species that have been assigned to a single species.

Cryptic species: two or more species that are morphologically

identical/similar.

Spatial heterogeneity in climate and topography

Images by Deepak V.Additional layers: Soil and temperature map

Much of species identification and description based on morphology.

This is a problem because one cannot distinguish cryptic species

morphologically.

How do we delimit (cryptic) species?

Issue with species complex

How do we delimit (cryptic) species?

What is a species?

Ernst Mayr (1942) species problem

Over 20 species concepts

Morphological (or Phenetic) Species Concept (MSC) Morphospecies

-Members of a species are morphologically similar to each other,

Fixed character difference (taxonomists).

Biological Species Concept (BSC)

-Individual that are interfertile belong to the same species

Ecological Species concept

Set of organisms exploiting a single niche (adaptive zone)

Species concepts

Set of organisms exploiting a single niche (adaptive zone)

Phylogeny-based concepts

-Evolutionary species concept (ESC)

A lineage evolving independently

-Phylogenetic species concept (PSC)

Smallest diagnosable monophyletic group

-genealogical species concept (GSC)

Mutually monophyletic in the genealogies of all genes

Lineage species concept (LSC)=General concept of species (GCS)

de Queiroz (1998, 2007), noted that the various species concepts

(such as BSC, PSC, ESC etc) are related to diversity of events or

subprocesses that occur during speciation and that all modern species

definitions are variations of the same general species concept which

he calls the lineage species concept or general concept species.

Species are segments of separately evolving metapopulation lineages.

Lineage refers to an ancestor-descendant Lineage refers to an ancestor-descendant

series, in this case of metapopulations or

simply a metapopulation extended through

time.

Metapopulation refers to an inclusive

population made up of connected

subpopulations.

Thus, under all species concepts, a species is a separately evolving

metapopulation lineage,

but under the isolation version of the biological species concept, the lineage

also has to be intrinsically reproductively isolated from other lineages;

under the ecological species concept, the lineage also has to occupy a

different niche;

under the phenetic species concept, it also has to be pheneticallyunder the phenetic species concept, it also has to be phenetically

distinguishable;

under the phylogenetic species concept (monophyly version), it also has to

be monophyletic in terms of its component genes, organisms, or

subpopulations, and so forth.

The diversity of events or subprocesses that occur during speciationdo not always occur in the same order.

How do we delimit species? Presence of any one of the properties (subprocesses) is evidence for the existence

of a species, though more properties and thus more lines of evidence are

associated with a higher degree of corroboration (de Queiroz, 2007).

The actual demarcation of species taxa uses morphological, geographical,

ecological, behavioral, and molecular information to infer the rank of isolated

populations (Ernst Mayr, 1996)

Multiple lines of evidence, multi-dimensional approach

Integrative taxonomy!

MD RI ED

Integrative taxonomy!

1) Morphological divergence MD (MSC)

2) Ecological divergence ED (Ecological SC)

3) Reproductive isolation RI (BSC)

4) Reciprocal monophyly RM (PSC)

5) Behavioral divergence BD (such as call, RSC)

BD RM

MD

BD

RI

RM

“Good species”

ED

Lineage species concept/ Integrative taxonomy

and

Indian systems

S. hypoleucos

S. entellus

Semnopithecus

complex

S. priam +

S. johnii

Mitochondrial

Cytochrome b tree

NJ/MP/Bayesian

approaches

S. entellus

S. hypoleucos

Nuclear NJ tree based

on four markers

S. johnii

S. priam

Ashalakshmi C.N

on four markers

Hemidactylus brookii complex

Aparna Lajmi

Sitana ponticeriana complex

Deepak V.

Late Cretaceous diversification among peninsular Indian centipedes

suggest their Gondwanan origin

Cormocephalus

Scolopendra

Digitipes COI, 12S rRNA

28S rRNA

Rhysida

Ethmostigmus

CretaceousJurassic Tertiary50100150200

Jahnavi JoshiMYA

28S rRNA

Likelihood tree

Digitipes species complex

mtDNA tree Nuclear DNA tree Separation on Env. axis (PCA) Morphology tree Traditional Taxonomy

Species 1 √ χ √ χ# D. coonoorensis

Species 2 √ χ √ χ+ D. indicus

Species 3 √ χ √ √ cf D. barnabasi

Species 5 √ √ χ χ# cf D. coonoorensis

Species 6 √ √ χ χ# cf D. coonoorensis

Species 7 √ √ √ √ cf D. barnabasi

Species 8 √ √ √ √ D. barnabasi

Group D Species 9 √ √ NA χ+ D. sp

Group A

Group B

Group C

1a1a

1b1b

22

How to detect and delimit cryptic species

Species 1 consists of 2 species (a,b) ?

Intraspecific population structure?

Cryptic species

3

3

Use speciation models to detect putative species

Rosenberg’s P, PTP, Bayesian approach

Integrative taxonomy, multiple lines of evidence

Species complexes from the Indian subcontinent

TT IT Reference

Primates

Semnopitheus 3 6 Ashalakshmi et al. (2015)

Reptiles

Sitana 1 >18 Deepak et al. (in prep.)

Geckoella 7 14* Agarwal & Karanth (2015)

H. brookii 1 5 Lajmi et al. (submitted)

C. aravallense 1 7* Agarwal et al. (2014a)

Cyrtodactylus(I) 5 22* Agarwal et al. (2014b)Cyrtodactylus(I) 5 22* Agarwal et al. (2014b)

Amphibians

Raorchestes 43 52(9) Vijayakumar et al. (2014)

Invertebrates

Digitepes 3 6 Joshi & Karanth (2012)

Itaropsis 1 >3 Jaiswara et al. (2012).

TT: Traditional taxonomy

IT: Integrative taxonomy

*Molecular data suggests multiple species

Implications

Widely distributed species might be a

species complex

Cautionary note: interspecific rather than

Intraspecific comparison, example Hanuman langur

Application of new methods for diagnosing species

Morphology as the sole criteria for species description obsoleteMorphology as the sole criteria for species description obsolete

Acoustic, behavioural, anatomical, skeletal, chromosomal,

olfactory cues (chemical) and molecular data

Diversity under estimated

Next frontier in biodiversity research in the tropics?

What groups to target?

Invertebrates (need not be widely distributed), small widely distributed vertebrates

Dispersal ability might be important

Newton 1988