Evolutionarily Significant Unit
G4
G6 & G7
G5
G8 & G9
The Maculinea alcon-rebeli debate
M. alcon and M. rebeli:
Host ants diversification in Maculinea population
G10
Maculinea arion: the genetic approach
G11
Conclusion
The case of Maculinea butterflies
When taxonomic variability does not reflect biological diversity in butterflies
Although identifying species is easy after molecular studies have been introduced, however, some cases in the identification of species by several authors cited did not reflect on the ESU paradigm.
G3
The ESU: Some insights from butterfly studies
G1 & G2
Inhabit very distinct biotopes
Sometimes considered one of the best example of “ecological races” among cuckoo species
Extinct in:
- Netherlands, 1964 (Tax, 1989)
- United Kingdom, 1979(Thomas, 1995)
- Belgium, 1996 (Goffart, 1997; Thomas et al., 2009)
Extinction in UK:
- Shows that comprehensive ecological, demographic & genetic understanding of (threatened) species is necessary for an effective conservation strategy (Thomas et al.,2009).
M. arion
- Listed as endangered species by IUCN (van Swaay et al., 2010)
- Listed in Annex IV of the Habitats Directive
- Important indicator of habitat quality,
- Umbrella species for several peculiar kinds of grassland communities (Randle et al., 2005; Spitzer et al., 2009; Casacci et al., 2011).
Show distinct ecological preferences
Confusion in intraspecific taxonomy of European populations of the M. arion. Bereczki et al. (2011) had contrast in two ecotypes in Carpathian region.
Maculinea arion ligurica (Wagner, 1904)
- Taxon was described in northwest Italy
- Flight occurs from end-June to mid-August
- Usually in xerothermic areas
- Lay eggs on Origanum flowerhead (Patricelli et al., 2011).
Maculinea arion arion (Linnaeus, 1758)
- Fly from mid-May to mid-June
- Favours short-grass dry fields
- Initial food plant is mostly Thymus spp.
Criteria used in defining ESUs was not fulfilled in Carpathian populations
- Two M. arion population groups were not isolated according to the basis of allozyme studies.
- Observation showed that there was overlapping at a certain level in their larval food plants, leading to the idea of ecological isolation between the two groups to weaken.
Priority should be recognised for species showing the highest character richness in phylogenetic reconstructions
Limiting the field to those taxa that are grossly and obviously independent on morphological or molecular bases would result in a wholesale sell-out of the dynamics of our biodiversity
Taxonomy ultimately teaches us that the conservation unit's diagnosis should fully recognize multiple forces capable of driving evolution of molecular, ecological, morphological and behavioral characters.
Maculinea alcon alcon and Maculinea alcon rebeli are considered as:
Maculinea alcon and Maculinea rebeli are considered as:
Separation of species based on ecological criteria (host ant species, habitat, initial larval food plant) and behavioural criteria (caterpillar’s growth rate & adult phenology)
ASPECT
Ecological
Behavioural
Variations in caterpillar’s growth rate & adult phenology
Habitat
Initial larval food plant
M. alcon
➜ Gain most of their weight in the late spring of the following year.
➜ Accelerate their development after diapause to obtain the optimal timing of adult emergence of G. pneumonanthe.
M. rebeli
➜ Acquire G. cruciata about half of their final body mass before
overwintering.
M. alcon
➜ Wet meadows
M. rebeli
➜ Adults inhabit dry grasslands
M. alcon
➜ Molinia caerulea (L.) Moench
➜Females primarily oviposit on Gentiana pneumonanthe L.
M. rebeli
➜ Gentiana cruciata L.
Butterflies represent a
good indicator group for other insect taxa
Butterflies possess well-known ecological preferences and react much more strongly and more rapidly to the behaviour of the drivers of change than other well-studied taxa.
Some butterflies have been found extinct even though have enough resources to survive.
On leaving its food plant, M. reveli secretes a simple mixture of surface hydrocarbon that weekly mimic those of its host Myrmica ants
Genetically the species are distinct but it cannot be classified into different ESU due to less in ecological distinctness.
Two or more species might be classified into a single ESU based on the knowledge of their biology and adaptive restrictive definitions.
Despite having different habitat preferences, the two ecotypes can locally co-occur while being phenologically isolated.
Differentiation in phenology and habitat preference constitutes conservation value despite not considered as separate ESUs
It is sufficiently similar to all other Myrmica species for the larvae to be quickly retrieved by the first ant worker coming by
The intruding larvae successfully blend within populations of the model host species by integrating additional hydrocarbons that are more accurately imitate their Myrmica host (Schönrogge et al. 2004; Witek et al. 2013)
Caterpillars adopted within nests of Myrmica species by contrast, suppress their productions and depend on the passive acquisition of their current host colony odour (Schönrogge et al. 2004)
Camouflage alone is an insufficient mechanism to survive inside the populations when worker ants become more discriminating
Host specificity patterns
- Myrmica schencki most frequently used as a "primary" host by M. rebeli in population investigation.
- Shift towards new Myrmica species.
- "coevolutionary hotspots" where the parasite hangs in balance between two host species as differentiation is in progress.
Ants & Cuckoo
Cuckoo inhabit ants’ brood chambers and
become highly integrated with their host society
Cuckoo receive grooming and are fed by the nurse ants, mainly by trophallaxis (cuckoo feeding)
suggested to be undergoing rapid ecological divergence
The populations use as hosts more than 10 Myrmica species all across their European distribution
Large number of host switches. Individual populations are typically highly species-specific with respect to ant association
Subspecies or Formenkreis of a single species with indistinguishable adult morphologies and genitalic characters.
Genus Maculinea
M. arion, M. teleius, M. nausithous, M. alcon, M. rebeli
obligate social parasites
model system for studies in the field of evolutionary ecology
survivability of Maculinea larvae depend on specificity of food plants and ant species
Larvae spends 11/23 months inside host colonies by adoption through chemical deception of host ants by chemical and acoustical cues
Make use of different feeding strategies once in ant colony
"cuckoo feeders"
larvae being fed by worker ants by trophallaxis)
"predatory species"
M. alcon & M. rebeli
prey on ant brood
M. arion & M. teleius
M. nausithous (not fully clarified)
coexistence of "cuckoo" and "predatory" strategies
predominance of "cuckoo" behaviour
Most of the distribution of Maculinea sp. is severely declining
Gained wide public attention due to
endangered status
extraordinary life history
Listed in Annexes II & IV of European Habitats Directive
Cuckoo Lifestyle
Main cost
increased specialization restricts each social parasite
to a smaller, regional part of its host range.
extremely complex, as a consequence of local adaptations
Genetic structures of 20 M.arion populations from two distinct and geographically distant parts of Europe
Poland population - Occupy xerothermic grasslands on the southerly exposed slopes and exploit Thymus spp
Italy population - Three morpho-ecotypes are present and colonised high-altitude pastures and exploit Thymus spp.
Declarations to the effect that should be concentrate our scarce resources to protect only the most sharply defined taxa are in sheer opposition to the ESU concept.
When under stress (eg. food shortage), they are able to distinguish between host and parasite larvae thus killing the parasite due to host high level of specificity (Elmes et al. 2004).
ESU and other related concepts
Evolutionary Significant Unit
• Definitions by some other authors (Waples 1991; Dizon et al. 1992; Vogler & Desalle 1994; Bowen 1998) tend to overlap with subspecies concepts.
• Some recent works, considering the ever-increasing availability of genetic data, have suggested, or sometimes even tended to force, the adoption of criteria exclusively based on molecular phylogenies, while largely ignoring all other otherwise measurable adaptive components (Avise 1994; Moritz 1994a,b).
• Traditionally, judgements on how distinctive a population should be, before it becomes eligible for being recognised as an ESU, were based on ecological as well as on variously measurable genetic information, thereby trying to take into account its effective evolutionary distinctness (see definitions by Ryder 1986 but also Crandall et al. 2000 in Table I).
• Here we have a theoretical issue, because although mainstream notions of speciation mechanisms include evolution of separate adaptations in allopatric or peripatric conditions (see Mayr 1963; Provine 2004 for reviews), the ESU concept, which implies demonstrable adaptation, does not necessarily overlap, or cannot necessarily be applied, to every separate segment in a phylogenetic tree, whose divergence may be a consequence of other genetic mechanisms, unless otherwise demonstrated.
• All ESU definitions possess both strengths and bits of weakness, authors have argued that differing approaches may work more efficiently than others, depending on cases and circumstances. This implies that designating ESUs should be done flexibly, on a case-by-case basis (Fraser & Bernatchez 2001).
• Strictly speaking, populations or taxa apparently characterized only by genetic divergence should better be considered Conservation Significant Units (CSUs) (see Yuan et al. 2011) rather than ESUs.
• Some authors have suggested that obtaining a fixed and universal definition of ESU, valid across all species, may not be feasible (e.g. Fraser & Bernatchez 2001).
Evolutionarily Significant Unit (ESU) definitions since Ryder (1986)
Ryder (1986) - state basic definitions: Population units presenting significant adaptive variation based on concordance between sets of data derived by different techniques (life history information, morphometric, range and distribution data, and genetic data)
Definitions stressing the importance of molecular data
Definitions stressing the importance of using molecular analysis and ecological data
Dizon et al. (1992) - Populations exhibiting discontinuous genetic divergence patterns, geographic isolation and significant genetic distances
Moritz (1994a,b) - Populations that are reciprocally monophyletic for mtDNA alleles and demonstrate significant divergence of allele frequencies at nuclear loci
Bowen (1998) - Populations which show evidence of long-term isolation
Fraser and Bernatchez (2001) - A lineage demonstrating highly restricted gene flow from other such lineages within the higher organizational level of the species
Vogler and Desalle (1994) - Groups that are diagnosed by characters which cluster individuals or populations to the exclusion of other such clusters
Waples (1991) - A population or group of populations that: is substantially reproductively isolated from other conspecific population units; represents an important component of the evolutionary legacy of the species
Crandall et al. (2000) - Prefer identification of distinct populations characterized by genetic and ecological inexchangeabilities over recent and historical times
De Guia and Saitoh (2007) - Full ESUs can be defined solely when information about both neutral genetic variation and adaptive variation is available; otherwise the taxa are ascribed to partial ESU
ESU: conservation unit below the species level, theoretically applicable to various taxa
ESU Conception: design to provide a theoretical background for prioritizing taxa
Field: conservation management, economic, genetic diversity
ESU might be fully identical with a "species". A "species" could be compose of multiple ESU. ESU lineage include single or multiple population and exchanging a degree of gene flow
"Species" concept was adapting in ESU
Aim : To define an identical "entity" whose divergence can be measured or assessed by placing differential emphasis on the role of evolutionary forces at different time scales
There is genetic differentiation in both COI and EF-1 alpha nuclear gene.
There is almost no mtDNA polymorphism found.
host specificity pattern in M. rebeli and M. alcon
Major different in chemical profiles could be use to trace host shift (Thomas et al. 2013)
Other approaches
Important, related concepts
Some countries are trying to protect so-called Independent Conservation Unit (ICU) instead of species
USA: Endangered Species Act makes references to "species" in Distinct Population Segments (DPS) that is applying pragmatic basis
DPS should be reproductively at least partially isolated by some physical barrier
Some authors/state agencies make reference of DPS respect to ill-defined ESUs
Can encompass all conservation needs such as protect population of harvested species and prevent extinction
The term "unit" refers to individual population
To protect all populations of any given species, the restricted number of local population needs to be focused on
Introduction
In conservation biology, protect a "species" is the most important
Different countries or geographical areas define "species" differently
Field study (Elmes et al. 2004) and an analysis of
pre-adoption chemical profiles (Nash et al. 2008)
Suggested
Evolution between European form of M. alcon (that exploits Myrmica scabrinodis) and
that of Scandinavia and Netherlands, which is adapted to Myrmica rubra/M. ruginodis had similar differentation.
Ant association
a double-edged sword
for the conservation of lycaenid butterflies
- promoted rapid rates of diversification
- creating a mosaic of overlapping ant and
plant hosts - produced small, isolated noninter-exchangeable populations
This condition leads to speciation however increase in fragmentation due to anthropogenic disturbances and habitat loss may dramatically increase the risk of local extinction
Molecular level
Local host ant adaptations
- detectable only by markers linked with genes under selection by specific aspects of social parasitism
- extremely important tgar myrmecophilous insect populations exploiting different host ants reognised as separate ESUs
Case of Maculinea arion in United Kingdom
- Species went extinct (1979)
- Due to the host ant was replaced by unsuitable congener species, unable to support the caterpillars of the parasite with modest changes in grazing regimes and vegetation structure (Thomas et al. 2009)
Clear separation of M. rebeli and M. alcon
Italian population of M. rebeli and M. alcon indicate distinct phenological differences between them based on:
Note: Phenology is the scientific study of periodic biological phenomena, in relation to climatic conditions
On the wing (from mid-June till mid-July and end of July to end of August)
Choices made by adult butterflies during oviposition
Host ant species
The unresolved taxonomic status of M. rebeli and M. alcon
Are they from separate clade?
Some unpublished data from larval epicuticular hydrocarbons support their differentiation, however other molecular studies based on sequence data of nuclear and mtDNA or on allozymes unable to separate them.
From recent molecular research in Poland and Lithunia, the issue on their conservation status is reopened again.
The analysis of nuclear EF1-a gene was insufficient for taxonomic classification.
Combining EF1-a gene and the microsatellite information manifest three ESUs.
corresponding to population of M. alcon and two geographically separated of M. rebeli.
Each species deserve specific conservation measures.
Are they severely threatened?
Yes, habitat patches of these species are becoming more isolated due to:
What is the status in the Appendixes and Annexes to the Bern Convention and to the EU Habitats Directive?
Abandonment of previous agricultural practices.
Light grazing in controlling soil erosion.
Deforestation.
Climate change.
Environmental fragmentation.
M. alcon is more threatened at southern limits of its range, especially in Italy.
Sinking water table.
M. rebeli needs more conservation actions in northern Europe compared to M. alcon.
Due to unresolved taxonomic status:
Not listed as threatened species with extinction in Europe.
Failed to find evidence for clade-level separation between M. alcon and M. rebeli.
- High degree of polymorphism & divergence
- Able to survive glaciations
Posglacial re-colonisation area
- Relevance in the context of biodiversity conservation
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