404 - Page Not Found!
404logo.jpg

Main issue

Our work aims to answer the question: "Is ecological specialization always an evolutionary dead-end"?

Overview

Evolutionary specialization occurs when an organism is capable of optimally using a narrow fraction of the resources available. It is usually a result of competition or coevolution. Specialized organisms frequently have phenotypic traits (e.g. morphological, physiological, behavioural, molecular or a combination of thereof) which permit an optimal exploration of the resources on which they are specialized. A controversial topic is whether the evolution of such traits makes it difficult for specialist clades to give rise to generalist ones. This review aims to abridge the studies that have addressed to explain the evolutionary patterns of generalization and specialization.

Introduction

Specialist organisms utilize only a subset of suitable and available resources, while generalist species use a wide array of resources (Futuyma & Moreno 1988) depending on the environmental resource availability. The evolution of specialization is often coupled with the appearance of phenotypic traits that optimize the use of a specific kind of resource. On the other hand, once an organism becomes specialist, it gets trapped in the ecological niche and loses the ability to explore other types of resources as efficiently as before. Thus, there is a trade-off between the ability to explore a wide variety of resources and the efficiency in using each one of them (Futuyma & Moreno, 1988) imposed by the phenotype. Specialization may arise in different morphs of the same species (e.g. Meyer, 1989) or among different species (e.g. flower-visiting insects that explore either pollen or nectar, Krenn et al. 2005; spiders that feed on woodlice employ different grasping tactics, Rezác et al. 2008). Species exploring similar resources often have similar phenotypic modifications even if they are not phylogenetically related.

Many factors have been proposed to explain the evolution of specialization as a habitat-specific adaptation (e.g. Schluter 1993, 1995; Joshi & Thompson 1995), competition for resources (MacArthur & Levins 1964), predator evasion (e.g. Bernays & Graham 1988; Bernays 1989) and mate-finding. Many of these factors have involved the modification of morphological structures, changes in feeding habits or in the case of symbiotic species several types of host selection. These changes enhance the competitive ability so that specialists are predicted to have higher fitness in their native environment than do plastic generalists (Donohue et al. 2000).

One of the most controversial and debatable topics in evolutionary biology is regarding to the evolution of specialists and generalists. Ecological specialization is often described as a derived state where further diversification is hampered, representing thus an “evolutionary dead-end” (Futuyma & Moreno 1988; Moran 1988; Kelley & Farrel 1998). This theory is based on the assumption that highly specialized structures or organisms will rarely evolve into a new structure or give rise to another species (Holmes 1977). Generalist species on the other hand could be more likely to diversify into specialists ones.

Here, we present scenarios and mechanisms of specialization that do not lead to an evolutionary dead-end. We employ a phylogenetic approach to understand if generalists always give rise to specialists or whether specialists have also resulted in generalist clades, indicating a shift of specialization to generalization.

Is there phylogenetic evidence for ecological specialization being an evolutionary dead-end?

Futuyma & Moreno (1988) suggested definition of specialization and generalization in reference to particular axes of ‘n-dimensional’ hypervolume; where environmental variables or resources form the axes. Ecological specialization is hard to define quantitatively because the specialist-generalist spectrum is a continuum trait. Hence, we define specialized species by comparing their range of resource use with that of closely related species. This highlights the importance of studying specialization in a phylogenetic framework.

We assessed a number of phylogenies (Table 1) of different groups of organisms containing varying degrees and types of specialization (such as host plants, feeding behaviour, habitat type, etc.) highlighting scenarios that do not lead to an evolutionary dead-end. Three of the 23 phylogenies we analysed were consistent with the idea that specialization leads to an evolutionary dead-end (e.g. Fig. 1A), while most other scenarios (15) indicated the diversification of specialists into the generalist clades (e.g. Fig. 1B). However, in five of the phylogenies we analysed the specialists occupied the tips of the tree because of the recent divergence and hence were not ideal for such comparisons. In some of the aforementioned cases, the authors suggest that some ways of specialization may lead to an evolutionary dead-end (moth- and bat-pollination), while others do not (humming bird-pollination; Tripp & Manos 2008). In some of these cases pertaining to host range evolution, the generalists were repeatedly derived from specialist lineages and occupied terminal branches of the phylogeny. Some authors suggested that the parasite and parasitoid generalist lineages may be less likely to diversify due to few opportunities of genetic isolation (Stireman 2005).

It is difficult to discern why a few specialist clades in a phylogeny diversify into generalists while others don’t. The degree of specialization has a greater impact on the ability of the specialist to reverse to the ancestral state. Here we discuss several mechanisms that could explain why and how ecological specialization can be reversed.

Mechanisms of reversal to generalization

1. Character loss, gene expression and re-evolution of ancestral characters.
Specialization often leads to the reduction or complete loss of morphological features. According to the Dollos’ law the reappearance of complex features could be nearly impossible. The theory is based in the assumption that after a structure is lost the genes related to it would degenerate (Gould 1970; Kohlsdorf and Wagner 2006). Therefore, it is important to understand whether a gene is lost completely or if it is present but remains unexpressed.

The reduction and loss of limbs in some reptiles has evolved several times and is often associated to specialization towards a burrowing behaviour (Kohlsdorf & Wagner 2006, but see Wiens & Slingluff 2001). The expression of Hox genes is responsible for patterning and limb positioning during tetrapod embryonic development (Burke et al. 1995; Shubin et al. 1997). Limb development and hox gene expression patterns therefore constitute a good model for testing the hypothesis that specialization is an evolutionary dead-end.

The reversibility of digit loss was documented for newts (Wagner et al. 1999). This study shows that the expression of the Hoxa-11 gene in Xenopus is similar to those described in chick and mice while in the newt Notophthalmus has an autopodial expression of the Hoxa-11 gene. Their results suggest that the postaxial digits in urodeles may be evolutionary innovations probably arising from an ancestor with reduced digits (Wagner et al. 1999). The reversibility of digit loss was also reported for Gymnophthalmidae (Kohlsdorf and Wagner 2006). A study regarding the morphological transition from lizard to snakelike body forms in reptiles however indicates that the digit loss was never recovered in the studied group (Wiens & Slingluff 2001). The reduction and loss of the digits might have occurred multiple times in evolution in a gradual way. The results suggest for a gradual evolution towards limb reduction which is neither necessarily associated to burrowing behaviour nor with the expression of the hox gene (Wiens & Slingluff 2001). The implications of these unexpected results for specialization and gene expression should be further explored. In summary, there is clear evidence for evolutionary reversals at the gene-expression level, indicating that specialization is not an evolutionary dead-end. Genes related to development seem to be highly conserved and do not disappear with a morphological innovation (Carroll et al. 2001). Hence, the factors regulating their expression and the time necessary for a character re-evolution still needs to be clarified.

2. Obligatory versus Facultative Specialization
It is widely believed that specialist species decline and experience higher extinction rate relative to the generalist counterparts (Clavel, Julliard & Devictor). It is the very “jack of all trades is a master of none” nature of generalists that seems to be conferring them the ability to adapt when the resource they depend on depletes (McKinney 1997; Devictor et al. 2008; Colles, Liow & Prinzing 2009). Contrastingly, the specialist species are considered to be so adapted to exploit the narrow range of resource they depend on that they cannot switch to a different type of resource when confronted by the aforementioned scenario of resource depletion.

For a long time ecological specialization was most often considered to be accompanied with the limitation of niche breadth, resulting from evolutionary trade-offs between the ability of species to exploit a range of resources and their capacity to use each one (the ‘jackof-all-trades is master of none’ hypothesis; MacArthur 1972). Though this seems like a more plausible scenario, there are specialist organisms that do not follow this rule and restrict their specialization to a narrow range resource; for instance, although phytophagous insects are extremely adapted to feed on plants, some species could feed on an array of plants.

Aipysurus eydouxii (marbled sea snake) is yet another interesting example of a facultative specialist. Although most sea-kraits are equipped with a deadly arsenal of venom, A. eydouxii has lost its ability to produce venom because of its switch of diet from fish to fish-eggs (Glodek & Voris 1982; H. K. Voris & H. H. Voris 1983). It is so highly evolved for eating fish-eggs that it has even lost the fangs and its venom glands have greatly atrophied (McCarthy 1987; Gopalakrishnakone & Kochva 1990). Despite the greater degree of specialization, A. eydouxii feeds on the eggs of a broad range of fish and hence is not dependent on a single species for survival. Facultative specialization might decrease the risk of extinction relative to obligatory specialization as the organism will not be dependent on narrow range of resources or a smaller niche breadth.

3. Role of phenotypic plasticity, sloppy fitness space and correlation trait evolution
One of the most obvious and intriguing features of parasitism is the pronounced conservatism in the range of host usage (high host-specificity), both on ecological (Thomson 1994, 2005) and evolutionary time-scales (Ehrlich & Raven 1964, Futuyma & Mitter 1996, Winkler & Mitter 2008). Many authors suggest that the host specificity holds the key to understand the evolution of host-parasite associations.
Agosta & Klemens (2008) proposed a general framework for ecological fitting as a mechanism behind the assembly of ecological communities and the formation of novel interactions between species within communities. They propose three factors leading to ecological fitting and the ability of the organisms to achieve realized fitness under novel conditions. First, phenotypic plasticity can allow organisms to mount a response to novel conditions (West-Eberhard 2003). Second, correlated trait evolution (Lande & Arnold 1983) can produce phenotypes that are ‘pre-adapted’ to some future novel conditions. Third, phylogenetic conservatism in traits related to resource use including design constraints (e.g. Gould & Lewontin 1979) and retention of traits from past selection pressures (e.g. Jansen & Martin 1982) that provide the latent ability to perform under apparently novel conditions: for instance, a parasite encountering a new host that is actually the same or sufficiently similar to some ancestral host (Brooks & Mc Lennan 2002). This leads to organisms possessing potential fitness outside the range of conditions in which the species evolved. Agosta & Klemens (2008) termed this region of fitness space “Sloppy fitness space”, a by-product of direct selection under some other set of conditions, the ancestral operative environment. It comprises all components refining a host as resource and therefore the range of host-related variables affecting parasite evolution (Fig. 3).

Host shift not only requires the acquisition of new traits to exploit the new host species but also often results in the loss of traits that were required to infect the ancestral host. The extent to which such modification will happen will depend on both local circumstances and evolutionary history. The butterfly Pieris napi regularly oviposit on the introduced plant Thalaspi arvense, despite the latter being lethal to the larvae (Chew 1977) and strangely, this process has not changed (Agosta et al 2010). Fox et al (1997) reported that initial colonization of Chloroleucon ebano by the seed beetle Stantor sp. depended on pre-existing variance in the capability to utilize this novel host. These aforementioned examples signify that successful host shifts depend on the history of the association as well as on the life history, abundance and distribution of the species.

4. Horizontal transfer
Illegitimate recombination or horizontal gene transfer (HGT) leading to the insertion of new DNA sequences could enhance the ecological niche of a bacterial species through the acquisition of new metabolic capabilities (Jain, R. et al. 2003). The addition of a new DNA fragment through HGT could promote speciation among bacterial lineages, as this would lower the rate of homologous recombination among initially promiscuous lineages (Vetsigian, K et al. 2005). Nitrogen-fixing bacteria that interact with leguminous plants belonging to the genus Medicago appear to be an ideal biological model for such studies (Bailly, X. et al. 2007). Phylogenetic analyses reveal that several interspecific horizontal gene transfers occurred during the diversification of Medicago symbionts. According to Bailly et al. 2007, incongruence between symbiotic and housekeeping gene phylogenies suggests that HGT of nod genes occurred between these two genera. In this context, the analyses performed up to now suggest that Sinorhizobium species acquired the ability to nodulate Medicago species through HGT of nod genes from the ancestor of a Rhizobium species, most probably R. mongolense (Bailly et. al. 2007). Bailly et al. 2007 say that horizontal transfer of nod genes might have occurred between S. meliloti and S. medicae after their speciation. Another example of HGT as source of capabilities for an organism is shown by Futterer et al. 2004, where they say that many genes that enhanced the abilities of Picrophilus torridus (an organism able to grow around pH 0 at up to 65°C ) to cope with its extremely acidic environment have been obtained by horizontal gene transfer. This includes some of the organic acid degradation pathways, the main components of the electron transport chain, and mechanisms to deal with oxygen stress. These examples show us that horizontal transfer is one of the mechanisms that could drive specialization. Gene acquirements can be reversed by high rates of non-neutral mutations, stochastic loss, deletions, post-transcriptional gene silencing, etc. Hence, ecological specialization can reverse to the ancestral generalized state.

Concluding Remarks

In this review we summarize several sources of evidence indicating that specialization does not always leads to an evolutionary dead-end. The re-evolution of morphological features related to generalization may happen in the reviewed circumstances: i) if the genes related to the generalist condition are not degenerated, ii) if the species is phenotypically plastic and iii) if the specialization degree is not high. Despite the wide diversity in the degree and type of specialization, it was possible to find a general pattern. We conclude that specialists are continually evolving and are not trapped in evolutionary dead-ends.

Table 1. List of phylogenies used to evaluate the hypothesis of evolutionary dead-end. Abbreviations as follow: (N) number of species used in the phylogeny; (N-spe) number of specialist; (Types of spec.) type of specialization: (H-phy: Host-phytophagous); (H-p: Host-parasitoids); (H-pa: Host-parasites); (H-m: Host-mutualist); (F: feeding); (H: habitat); (C: chemical); (P: pollinator); (G→S): transition from generalist to specialist; (S→G): transition from specialist to generalist; (S→S): specialist that explore different resources; Root: most plausible ancestor (G: generalist; S: specialist; U: unknown); (dead-end): Evidence of dead-end.

~Taxa ~N ~N-spe ~Type of spe. ~GS SG SS Root Dead-end References
Chrysomelinae (Coleoptera) 35 10 H-phy 2 1 0 G No Termonia et al. (2001)
Dendroctonus (Coleoptera) 19 6 H-phy 6 0 0 G Equivocal Kelley & Farrel (1998)
Timema (Phasmida) 17 17 H-phy 5 1 2 U No Crespi & Sandoval (2000)
Tomoplagia (Diptera) 19 19 H-phy 6 2 ? U No Yotoko et al. (2005)
Nymphalini (Lepidoptera) 26 13 H-phy 5 2 0 S No Janz et al. (2001)
Troidini (Lepidoptera) 33 5 H-phy 5 0 0 G Equivocal Silva-Bandrão et al. (2005)
Nymphalini (Lepidoptera) 26 15 H-phy 8 2 0 S No Janz et al (2001)
Parides (Lepidoptera) 33 4 H-phy 4 0 0 G Equivocal Silva-Bandrão et al. (2005)
Acrididae (Orthoptera) 13 8 H-phy 0 3 1 S No Rowell & Flook (2004)
Cotesia (Braconidae) 45 45 H-p 0 0 15 S No O'Connor (2011)
Hymenoptera ? ? H-p 1 ? ? U No Whitfield (1998)
Schistosoma (Trematoda) 23 23 H-pa 0 0 9 S No Brant & Loker (2005)
Dactylogerus (Trematoda) 51 51 H-pa 0 6 30 S No Simková et al. (2004)
Monogenea (Trematoda) 74 51 H-pa 0 10+ 0 U No Sasal et al (1999)
Tachinidae (Diptera) 49 39 H-pa 0 5+ 0 S No Stireman (2005)
Amphiprion and //Premnas (Perciformes) 8 2 H-m 1 1 1 S No Elliot et.al (1999)
Tylomelania (Gastropoda) 92 39 F 32 0 0 G Equivocal von Ritelen (2004)
Thamnophilidae (Passeriformes) 70 14 F 2 0 0 G Yes Brumfield et al. (2007)
Diadasia (Hymenoptera) 28 28 F 0 2 4 S No Sipes & Wolf (2000); Sipes & Tepedino (2005)
Araneae 224 50 F 31 0 ? G Yes Pekár et al. (2011)
Emydidae (Testudines) 64 23 F 7-8 2-3 0 G No Stephens & Wiens (2003)
Emydidae (Testudines) 64 58 H 2 1-2 1 S No Stephens & Wiens (2003)
Dendrobatidae 61 ? F / C 4 0 0 U Equivocal Darst et.al (2005); Santos et al. (2003)
Ruellia (Acanthaceae) 115 ? P ? ? ? S Yes/No Tripp & Manos (2008)
cladogram1.png

Fig. 1. Topology of a group of spiders (Araneidae), showing the transition from generalist ancestor (grey circles) to specialist species (filled circles) that are mostly specialized to feed on Lepidoptera.

cladogram2.png

Fig. 2. Ancestral character reconstruction for diet (a) and habitat use (b) of an ecological diverse group of turtles (Emydidae), based on molecular phylogeny. Diet specialist states (herbivorous and carnivorous) / generalist state (omnivorous). The analysis suggests that the ancestor of the group was a dietary generalist. Figure extracted from Stephens & Wiens (2003).

Slide1.jpg

Fig. 3. A schematic illustration show 2 dimension of the operative environment associated with fictional host resources (black circles). Sloppy fitness space can allow realized fitness in an area outside from the operative environment to which the parasite is adapted (light green circles). Panels a, d and g illustrate a specialist adapted to a single host resources, panels b, e and h illustrate a polyspecialist that has adapted independently to 3 different resources and panels c, f and i illustrates an generalist with a more general host recognition and tolerance system that allows it to utilize any resource that falls within the dark green area. The open circles in panels d-f represent 3 novel resources. The specialist in panel e can colonize resource 1 (which is more or less identical to de ancestral resource) but no resource 2 and 3. The polyspecialist in panel e can colonize resource 1, but also resource 2 that falls within its sloppy fitness space, and the generalist in panel f can colonize resource 1, but also resource 2 that falls within its sloppy fitness space, and the generalist in panel f can colonize all three resources. In panels g-i only host is available, and all three parasite species will appear to be specialists, but their ecological and evolutionary potential will be different.

References

Ackerly DD. 2003. Community assembly, niche conservatism, and adaptive evolution in changing environments.International Journal of Plant Sciences //, 164, 165–184.
Agosta, S.J & J.A. Klemens. 2008. Ecological Fitting by phenotypically flexible genotypes: implications for species associations, community assemble and evolution. //Ecology Letters //,11: 1123-1134.
Agosta, S.J., Janz N. & Brooks, D.R. 2010. How specialist can be generalist: resolving the “parasite paradox” and implications for emerging infectious disease. //Zoologia
27 (2):151-162.
Bernays E & Graham M. 1988. On the evolution of host specificity in phytophagous arthropods. Ecology, 69:886–892.
Bernays EA. 1989. Host range in phytophagous insects: the potential role of generalist predators. Evolutionary Ecology, 3:299–311.
Blackburn DG. 1984. From whale toes to snake eyes: comments on the reversibility of evolution. Systematic Zoology, 33, 241–245.
Brant SV & Loker ES. 2005. Can specialized pathogens colonize distantly related hosts? Schistosome evolution as a case study. PLoS Pathogens, 1, 167–169.
Brooks, D.R. & D.A. McLennan. 2002. The nature of diversity: an evolutionary voyage of discovery.University of Chicago.
Brumfield RT, Tello JG, Cheviron ZA, Carling MD, Crochet N & Rosenberg KV. 2007. Phylogenetic conservatism and antiquity of a tropical specialization: army-ant-following in the typical antbirds (Thamnophilidae). //Molecular Phylogenetics and Evolution
, 45, 1–13.
Burke AC., Feduccia A .1997. Developmental patterns and the identification of homologies in the avian hand. Science 278: 666–668.
Chew, F.S. 1977. Coevolucion of pierid butterflies and their cruciferous food plants. II. The distribution of eggs on potential food plants. Evolution51:1182-1188
Clavel, J., Julliard, R. & Devictor, V. (in press) Worldwide decline of specialist species: towards a global functional homogenization? Frontiers in Ecology and Environement.
Colles, A., Liow, LH. & Prinzing, A. 2009. Are specialists at risk under environmental change? Neoecological, paleoecological and phylogenetic approaches. Ecology Letters, 12:849–863.
Crespi BJ & Sandoval CP. 2000. Phylogenetic evidence for the evolution of ecological specialization in Timema, walking-sticks. Journal of Evolutionary Biology, 13, 249–262.
Darst CR, Mene PA, Coloma LA & Cannatella DC. 2005. Evolution of dietary specialization and chemical defense in poison frogs (Dendrobatidae): a comparative analysis. The American Naturalist, 165, 56–69.
Devictor, V., Julliard, R., Clavel, J., Jiguet, F., Lee, A. & Couvet, D. 2008. Functional biotic homogenization of bird communities in disturbed landscapes. Global Ecology and Biogeography, 17:252–261.
Donohue K, D Messiqua, E Hammond-Pyle, SM Heschel & J Schmitt. 2000. Evidence of adaptive divergence in plasticity: density and site-dependent selection on shade avoidance responses in Impatiens capensis. Evolution, 54:1956–1968.
Ehrlich, P. R. & P. H. Raven. 1964. Butterflies and plants: a study in coevolution.Evolution.18:586-608
Elliott JK, Lougheed SC, Bateman B, Mcphee LK & Boag PT. 1999. Molecular phylogenetic evidence for the evolution of specialization in anemone fishes. Proceedings of the Royal Society of London B: Biological Sciences, 266, 677–685.
Fox, C.W., J. A. Nilsson & T.A. Mousseau. 1997. The ecology of diet expansion in a seed- feeding
Futterer, O., Angelov, A., Liesegang, H., Gottschalk, G., Schleper, C., Schepers, B., Dock, C., Antranikian, G., and Liebl, W. (2004) Genome sequence of Picrophilus torridus and its implications for life around pH 0. Proceedings of the National Academy of Sciences of the United States of America 101, 9091-9096.
Futuyma DJ & Moreno G. 1988. The evolution of ecological specialization. Annual Reviews of Ecology and Systematics, 19:207-233.
Futuyma, D.J & C. Mitter. 1996. Insect-plant interactions: the evolution of component communities.Philosophical Transactions of the Royal Society of London, Series B351: 1361-1366.
Glodek, GS. & Voris HK. 1982. Marine snake diets: prey composition, diversity and overlap. Copeia, 3:661–666.
Goldberg EE & Igic B. 2008. On phylogenetic tests of irreversible evolution. Evolution, 62:2727-2741.
Gopalakrishnakone P. & Kochva E. 1990. Venom glands and some associated muscles in sea snakes. Journal of. Morphology, 205:85–96.
Gould, S. J & R. C. Lewontin. 1979. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme.Proceedings of the Royal Society of London, Series B.205: 581-598.
Gould, S. J. 1970. Dollo on Dollo’s law: irreversibility and the status of evolutionary laws. // Journal of the History of Biology, 3:189–212.
Holliday JA, Steppan SJ. 2004. Evolution of hypercarnivory: the effect of specialization on morphological and taxonomic diversity. Paleobiology. 30(1): 108-128.
Holmes EB. 1977. Is specialization a dead end? //American Naturalist
, 111:1021–1026.
Jain, R., M. C. Rivera, J. E. Moore, and J. A. Lake. 2003. Horizontal gene transfer accelerates genome innovation and evolution. // Mol. Biol. Evol. 20: 1598–1602.
Jansen, D.H. & P. S. Martin. 1982. Neotropical anachronisms: The fruits the Gomphotheres ate. Science215: 19-27
Janz N, Nyblom K & Nylin S. 2001. Evolutionary dynamics of host-plant specialization: a case study of the tribe Nymphalini. Evolution, 55, 783–96.
Joshi A & Thompson JN. 1995. Trade-offs and the evolution of host specialization. Evolutionary Ecology, 9:82–92.
Kelley ST & Farrell BD. 1998. Is specialization a dead end? The phylogeny of host use in Dendroctonus bark beetles (Scolytidae). Evolution, 52:1731–1743.
Kohlsdorf T & Wagner GP. 2006. Evidence for the reversibility of digit loss: a phylogenetic study of limb evolution in Bachia (gymnophthalmidae: squamata). Evolution, 60:1896-1912.
Krenn HW, Plant JD & Szucsich NU. Mouthparts of flower-visiting insects. Arthropod Structure and Development, 34:1-40.
Lande, R. & S.J. Arnold. 1995. Oviposition mistakes in herbivorous insects: confusion or a step towards a new host plant?.Oikos.72:155-160.
Leonard JA, Vilà C, Fox-Dobbs K, Koch PL, Wayne RK, Van Valkenburgh B. 2007. Megafaunal extinctions and the disappearance of a specialized wolf ecomorph. Curr. Biol. 17, 1146–1150.
Lombard RE, Wake DB. 1977. Tongue evolution in the lungless salamanders, family plethodontidae. II. Function and evolutionary diversity. 153: 39–79.
MacArthur RH & Levins R. 1964. Competition, habitat selection and character displacement in a patchy environment. Proceedings of the National Academy of Sciences, 51:1207–1210.
MacArthur, RH. 1972. Geographical Ecology. Harper & Row, New York, NY.
McCarthy, CJ. 1987. Adaptations of sea snakes that eat fish eggs; with a note on the throat musculature of Aipysurus eydouxi (Gray, 1894). Journal of Natural History, 21:1119–1128.
McKinney, ML. 1997. Extinction vulnerability and selectivity: combining ecological and paleontological views. Annual Review of Ecology and Systematic, 28:495–516.
Meyer A. 1989. Cost of morphological specialization: feeding performance of the two morphs in the trophically polymorphic cichlid fish, Cichlasoma citrinellum. Oecologia, 80:431-436.
Moran NA. 1988. The evolution of host-plant alternation in aphids: evidence for specialization as a dead end. American Naturalist, 132:681–706.
O’Connor JA. 2011. Phylogenetic patterns of host specialization in two tropical Microgastrinae (Hymenoptera: Braconidae) parasitoid wasp genera., Unpublished PhD Thesis, University of Illinois, 90pp.
Pekár S, Coddington JA & Blackledge TA. 2011. Evolution of stenophagy in spiders (Araneae ): evidence based on the comparative analysis of spider diets. Evolution, 66, 776–806.
Rezác M, Pekár S & Lubin Y. 2008. How oniscophagous spiders overcome woodlouse armour. Journal of Zoology, 275:64-71.
Richardson KC, Wooller RD (1990) Adaptation of the alimentary tract of some Australian lorikeets to a diet of pollen and nectar. Australian Journal of Zoology, 38, 581– 586.
rmonia A, Hsiao TH, Pasteels JM & Milinkovitch MC. 2001. Feeding specialization and host-derived chemical defense in Chrysomeline leaf beetles did not lead to an evolutionary dead end. Proceedings of the National Academy of Sciences of the United States of America, 98, 3909–3914.
Rowell CHF & Flook PK. 2004. A dated molecular phylogeny of the Proctolabinae (Orthoptera , Acrididae), especially the Lithoscirtae , and the evolution of their adaptive traits and present biogeography. Journal of Orthoptera Research, 13, 35–56.
Santos JC, Coloma LA & Cannatella DC. 2003. Multiple recurring origins of aposematism and diet specialization in poison frogs. Proceedings of the National Academy of Sciences of the United States of America, 100, 12792–12797.
Schluter D. 1993. Adaptive radiation in sticklebacks: size, shape, and habitat use efficiency. Ecology, 74:699–709.
Schluter D. 1995. Adaptive radiation in sticklebacks: trade-offs in feeding performance and growth. Ecology, 76:82–90.
Shubin NH. 1994. The phylogeny of development and the origin of homology. In: Grande L, Rieppel O, Eds. Interpreting The Hierarchy Of Nature. San Diego, CA. Pp201–225
Silva-Brandão KL, Freitas AV, Brower AVZ & Solferini VN. 2005. Phylogenetic relationships of the New World Troidini swallowtails (Lepidoptera: Papilionidae) based on COI, COII, and EF-1alpha genes. Molecular Phylogenetics and Evolution, 36, 468–83.
Simková A, Morand S, Jobet E, Gelnar M & Verneau O. 2004. Molecular phylogeny of congeneric monogenean parasites (Dactylogyrus): a case of intrahost speciation. Evolution, 58, 1001–1018.
Sipes SD & Tepedino VJ. 2005. Pollen-host specificity and evolutionary patterns of host switching in a clade of specialist bees (Apoidea: Diadasia). Biological Journal of the Linnean Society, 86, 487–505.
Sipes SD & Wolf PG. 2001. Phylogenetic relationships within Diadasia, a group of specialist bees. Molecular Phylogenetics and Evolution, 19, 144–56.
Stephens PR & Wiens JJ. 2003. Ecological diversification and phylogeny of emydid turtles. Biological Journal of the Linnean Society, 79, 577–610.
Stireman JO. 2005. The evolution of generalization? Parasitoid flies and the perils of inferring host range evolution from phylogenies. Journal of evolutionary biology, 18, 325–36.
Takahashi R, Watanabe K, Nishida M, Hori M. 2007.Evolution of feeding specialization in Tanganyikan scale-eating cichlids: a molecular phylogenetic approach. BMC Evolutionary Biology. 7:195
Tripp EA & Manos PS. 2008. Is floral specialization an evolutionary dead-end? Pollination system transitions in Ruellia, (Acanthaceae). Evolution, 62, 1712–1737.
Vetsigian, K., and N. Goldenfeld. 2005. Global divergence of microbial genome sequences mediated by propagating fronts. Proc. Natl. Acad. Sci. USA 102:7332–7337.
Villegas, M. D. C., S. Rome, L. Maure, O. Domergue, L. Gardan, X. Bailly, J. C. Cleyet-Marel, and B. Brunel. 2006. Nitrogen-fixing sinorhizobia with Medicago laciniata constitute a novel biovar (bv. medicaginis) of S. Meliloti. Syst. Appl. Microbiol. 29:526–538
von Rintelen T, Wilson AB, Meyer A & Glaubrecht M. 2004. Escalation and trophic specialization drive adaptive radiation of freshwater gastropods in ancient lakes on Sulawesi, Indonesia. Proceedings of the Royal Society of London B: Biological Sciences, 271, 2541–2549.
Von Rintelen T, Wilson AB, Meyer A, Glaubrecht M. 2004. Escalation and trophic specialization drive adaptive radiation of freshwater gastropods in ancient lakes on Sulawesi, Indonesia. Proc Biol Sci. 271: 2541–2549.
Von Rintelen, T. & Glaubrecht, M. 2003 New discoveries in old lakes: three new species of Tylomelania Sarasin & Sarasin, 1897 (Gastropoda: Cerithioidea: Pachychilidae) from the Malili lake system on Sulawesi, Indonesia. J. Moll. Stud. 69, 3–17.
Voris, HK & Voris HH. 1983. Feeding strategies in marine snakes: an analysis of evolutionary, morphological, behavioural and ecological relationships. American Zoologist, 23:411–425.
Wagner, GP., Khan, PA., Blanco, MJ., Misof, B. & Liversage, RA. 1999. Evolution of Hoxa-11 Expression in Amphibians: Is the Urodele Autopodium an Innovation? American Zoologist, 39, 686-694.
Wernegreen, J. J., and M. A. Riley. 1999. Comparison of the evolutionary dynamics of symbiotic and housekeeping loci: a case for the genetic coherence of rhizobial lineages. Mol. Biol. Evol. 16:98–113.
West- Eberhard, M. J. 2003. Developmental plasticity and evolutionOxford University Press, New York.
Whitfield JB. 1998. Phylogeny and evolution of host-parasitoid interactions in Hymenoptera. Annual Review of Entomology, 43, 129–51.
Wiens JJ. & Slingluff JL. 2001. How Lizards Turn into Snakes: A Phylogenetic Analysis of Body-Form Evolution in Anguid Lizards. Evolution, 55:2303–2318
Winkler, I. S. & C. Mitter. 2008. The phylogenetic dimension of insect-plant interactions: a review of recent evidence, p. 240-263.In: K. J. Tilman (Ed) The evolutionary biology of herbivorous insects: specialization, speciation and radiation Universidad de California, Berkeley.
Xavier Bailly, Isabelle Olivieri, Brigitte Brunel, Jean-Claude Cleyet-Marel, and Gilles Bena1 . 2007. Horizontal Gene Transfer and Homologous Recombination Drive the Evolution of the Nitrogen-Fixing Symbionts of Medicago Species . JOURNAL OF BACTERIOLOGY, July 2007, 189:5223–5236
Yotoko KSC, Prado PI, Russo CAM & Solferini VN. 2005. Testing the trend towards specialization in herbivore-host plant associations using a molecular phylogeny of /Tomoplagia, (Diptera: Tephritidae). Molecular Phylogenetics and Evolution, 35, 701–711.

Members

Asorey, Cynthia M. - PhD candidate, Universidad Catolica del Norte, Chile
Canales-Aguirre, Cristian B. - PhD candidate, Universidad de Concepcion, Chile
Kalsoom, Saima - PhD student, Quaid-i-Azam University, Islamabad, Pakistan
Kaminski, Valéria L. - Undergraduate student, Universidade Federal de Santa Maria, Brazil
Macias-Hernandez, Nuria- Post-doc, Aarhus University, Denmark
Magalhães, Ivan L. F. - Masters student, Universidade Federal de Minas Gerais, Brazil
Marcelino, Vanessa R. - Masters student, Ghent University, Belgium
Sunagar, Kartik B. - Phd candidate, CIIMAR/University of Porto, Portugal

Unless otherwise stated, the content of this page is licensed under Creative Commons Attribution-ShareAlike 3.0 License