Genital divergence in sympatric sister snails

A pattern of greater divergence in mating traits between sister‐species pairs with overlapping ranges than between allopatric species pairs is expected if reinforcement commonly contributes to speciation. Few large‐scale comparative analyses have addressed this prediction, especially for genital form. Here, we show that penial morphology follows the predicted pattern in 40 robustly identified sister‐species pairs in the marine gastropod subfamily Littorininae. Further work is needed to exclude other processes that may contribute to genital divergence between sympatric species, but the clear pattern we observe strongly suggests a role for genital form in reproductive isolation in this large clade.     

Experimental evidence that competition between stickleback species favours adaptive character divergence

The ecological character displacement hypothesis assumes that the effects of interspecific resource competition cause divergent selection to favour phenotypes that exploit non-shared resources. This model predicts that interspecific competition declines with increased divergence. Direct tests of this decline are rare despite much comparative evidence for character displacement. We tested this prediction using a pair of divergent brook sticklebacks. Brook sticklebacks sympatric with ninespine sticklebacks have diverged from local allopatric brook populations, and so the two types of brook sticklebacks potentially represent pre- and post-displacement forms. We used enclosures placed in a lake to compare short-term fitness (growth) of sympatric (post-displacement) and allopatric (pre-displacement) brook forms in the presence and absence of ninespine sticklebacks. Brook sticklebacks grew less in the presence vs. absence of ninespine sticklebacks, indicating that interspecific competition occurred. As expected, allopatric brook forms had lower growth than sympatric forms when ninespine sticklebacks were present. This result suggests that ecological character displacement has occurred.     

Species co-existence and character divergence across carnivores

Co-occurring species might be morphologically similar because they are adapted to the same environment, or morphologically dissimilar to minimize competition. We use sister species comparisons to evaluate the relationship between morphological disparity and regional patterns of co-occurrence across carnivores. Up to 63% of the variation in range overlap can be explained by morphological divergence in dentition. Species that differ more in carnassial tooth length overlap more in their geographical range. Carnassials are the primary teeth associated with food processing, and hence difference in carnassial size may be a good indicator of difference in resource use. We suggest this pattern is consistent with competition in sympatry driving ecological character displacement, or competitive exclusion among ecologically similar species. Our study uses newly available data on global distributions, morphology and phylogeny, and is the first to demonstrate a close relationship between morphological disparity and co-occurrence at a regional scale encompassing multiple communities.     

Parallel evolution and ecological selection: replicated character displacement in spadefoot toads

Ecological character displacement—trait evolution stemming from selection to lessen resource competition between species—is most often inferred from a pattern in which species differ in resource-use traits in sympatry but not in allopatry, and in which sympatric populations within each species differ from conspecific allopatric populations. Yet, without information on population history, the presence of a divergent phenotype in multiple sympatric populations does not necessarily imply that there has been repeated evolution of character displacement. Instead, such a pattern may arise if there has been character displacement in a single ancestral population, followed by gene flow carrying the divergent phenotype into multiple, derived, sympatric populations. Here, we evaluate the likelihood of such historical events versus ongoing ecological selection in generating divergence in trophic morphology between multiple populations of spadefoot toad (Spea multiplicata) tadpoles that are in sympatry with a heterospecific and those that are in allopatry. We present both phylogenetic and population genetic evidence indicating that the same divergent trait, which minimizes resource competition with the heterospecific, has arisen independently in multiple sympatric populations. These data, therefore, provide strong indirect support for competition''s role in divergent trait evolution.     

Location-specific sympatric morphological divergence as a possible response to species interactions in West Virginia Plethodon salamander communities

1. The competitive interactions of closely related species have long been considered important determinants of community composition and a major cause of phenotypic diversification. However, while patterns such as character displacement are well documented, less is known about how local adaptation influences diversifying selection from interspecific competition. 2. We examined body size and head shape variation among allopatric and sympatric populations of two salamander species, the widespread Plethodon cinereus and the geographically restricted P. nettingi. We quantified morphology from 724 individuals from 20 geographical localities throughout the range of P. nettingi. 3. Plethodon nettingi was more robust in cranial morphology relative to P. cinereus, and sympatric localities were more robust relative to allopatric localities. Additionally, there was significantly greater sympatric head shape divergence between species relative to allopatric communities, and sympatric localities of P. cinereus exhibited greater morphological variation than sympatric P. nettingi. 4. The sympatric morphological divergence and increase in cranial robustness of one species (P. nettingi) were similar to observations in other Plethodon communities, and were consistent with the hypothesis of interspecific competition. These findings suggest that interspecific competition in Plethodon may play an important role in phenotypic diversification in this group. 5. The increase in among-population variance in sympatric P. cinereus suggests a species-specific response to divergent natural selection that is influenced in part by other factors. We hypothesize that enhanced morphological flexibility and ecological tolerance allow P. cinereus to more rapidly adapt to local environmental conditions, and initial differences among populations have allowed the evolutionary response of P. cinereus to vary across replicate sympatric locations, resulting in distinct evolutionary trajectories of morphological change.     

Reproductive character displacement and speciation in periodical cicadas, with description of new species, 13-year Magicicada neotredecem

Abstract. Acoustic mate-attracting signals of related sympatric, synchronic species are always distinguishable, but those of related allopatric species sometimes are not, thus suggesting that such signals may evolve to "reinforce" premating species isolation when similar species become sympatric. This hypothesis predicts divergences restricted to regions of sympatry in partially overlapping species, but such "reproductive character displacement" has rarely been confirmed. We report such a case in the acoustic signals of a previously unrecognized 13-year periodical cicada species, Magicicada neotredecim , described here as a new species (see Appendix). Where M. neotredecim overlaps M. tredecim in the central United States, the dominant male call pitch (frequency) of M. neotredecim increases from approximately 1.4 kHz to 1.7 kHz, whereas that of M. tredecim remains comparatively stable. The average preferences of female M. neotredecim for call pitch show a similar geographic pattern, changing with the call pitch of conspecific males. Magicicada neotredecim differs from 13-year M. tredecim in abdomen coloration, mitochondrial DNA, and call pitch, but is not consistently distinguishable from 17-year M. septendecim ; thus, like other Magicicada species, M. neotredecim appears most closely related to a geographically adjacent counterpart with the alternative life cycle. Speciation in Magicicada may be facilitated by life-cycle changes that create temporal isolation, and reinforcement could play a role by fostering divergence in premating signals prior to speciation. We present two theories of Magicicada speciation by life-cycle evolution: "nurse-brood facilitation" and "life-cycle canalization."     

Phylogenetic relationships and ecomorphological divergence in sympatric and allopatric species of Paragalaxias (Teleostei: Galaxiidae) in high elevation Tasmanian lakes

Four species of Paragalaxias (Galaxiidae) inhabit lakes of submontane Tasmania. P. dissimilis and P. eleotroides are sympatric in Great Lake and Shannon Lagoon; P. mesotes occurs in Arthurs and Woods lakes; P. julianus is found in lakes of the Western Plateau. Phylogenetic analysis shows the genus to be monophyletic, and indicates that P. julianus is the sister-species of the other three species, and that P. dissimilis is the sister-species of P. mesotes and P. eleotroides. Morphological comparisons show that the two sympatric species have diverged from the others, with P. dissimilis becoming limnetic/pelagic (terminal mouth, eyes more lateral with convex interorbital, symmetrical paddle-shaped pectoral fins with rays divided once, forked tail, many, long gill rakers, large swimbladder), while P. eleotroides has become benthic (downturned mouth, eyes high on head with interorbital convex, rhomboidal pectoral fins with upper rays longest, rays divided twice, truncated tail, few, short gill rakers, small swim bladder). This character divergence is consistent with the tenets of character displacement except that it remains unproved that it has been driven by resource competition. The ecomorphological divergence parallels that described for species pairs in northern cool temperate lakes with fish faunas of low species richness, particularly in threespine stickleback, Gasterosteus aculeatus.     

How fluctuating competition and phenotypic plasticity mediate species divergence

Causal evidence linking resource competition to species divergence is scarce. In this study, we coupled field observations with experiments to ask if the degree of character displacement reflects the intensity of competition between two closely related spadefoot toads (Spea bombifrons and S. multiplicata). Tadpoles of both species develop into either a small-headed omnivorous morph, which feeds mostly on detritus, or a large-headed carnivorous morph, which specializes on and whose phenotype is induced by fairy shrimp. Previously, we found that S. multiplicata are inferior competitors for fairy shrimp and are less likely to develop into carnivores in sympatry with S. bombifrons. We compared four key trophic characters in S. multiplicata across natural ponds where the frequency of S. bombifrons varied. We found that S. multiplicata became increasingly more omnivore-like as the relative abundance of S. bombifrons increased. Moreover, in controlled laboratory populations, S. multiplicata became increasingly more omnivore-like and S. bombifrons became increasingly more carnivore-like as we increased the relative abundance of the other species. Phenotypic plasticity helped mediate this divergence: S. multiplicata became increasingly less likely to eat shrimp and develop into carnivores in the presence of S. bombifrons, a superior predator on shrimp. However, divergence also reflected differences in canalized traits: When reared under common conditions, S. multiplicata tadpoles became increasingly less likely to produce carnivores as their natal pond decreased in elevation. Presumably, this pattern reflected selection against carnivores in lower-elevation ponds, because S. bombifrons became increasingly more common with decreasing elevation. Local genetic adaptation to the presence of S. bombifrons was remarkably fine grained, with differences in carnivore production detected between populations a few kilometers apart. Our results suggest that the degree of character displacement potentially reflects the intensity of competition between interacting species and that both phenotypic plasticity and fine-scale genetic differentiation can mediate this response. Moreover, these results provide causal evidence linking resource competition to species divergence.     

An experimental test of character displacement's role in promoting postmating isolation between conspecific populations in contrasting competitive environments

Ecological character displacement takes place when two closely related species co-occur in only part of their geographical range, and selection to minimize competition between them promotes divergence in resource-use traits in sympatry but not in allopatry. Because populations sympatric with the heterospecific competitor will experience a different competitive environment than conspecific populations in allopatry, conspecific populations from these two competitive environments will also diverge in resource traits as an indirect consequence of interspecific ecological character displacement. Ultimately, ecologically dependent postmating isolation may arise between conspecific populations from these divergent competitive environments if offspring produced by matings between them are competitively inferior in either type of competitive environment. Yet, there are no direct tests of character displacement's role in initiating such postmating isolation. Here, we present a test by comparing the phenotypes and performances of spadefoot toad tadpoles produced from between-competitive-environment (BCE) matings versus those produced from within-competitive-environment (WCE) matings. When raised with naturally occurring competitors, BCE offspring grew significantly less and were significantly smaller than WCE offspring. BCE offspring generally performed worse even when raised alone, suggesting that they may have harbored intrinsic genetic incompatibilities. Moreover, the difference in growth and body size of BCE versus WCE offspring was significantly greater when each was raised with competitors than when each was raised alone, suggesting that BCE tadpoles were competitively inferior to WCE tadpoles. Presumably, this enhanced difference arose because BCE tadpoles produced an intermediate resource-use phenotype that is less well adapted to either competitive environment. Because larval size is under strong, positive, directional selection, reduced growth and size of BCE offspring may diminish gene flow between populations in divergent competitive environments, thereby generating postmating isolation. Thus, postmating isolation between conspecific populations, and possibly even speciation, may arise as a by-product of interactions between species.     

Metabolic divergence between sibling species of cichlids Pundamilia nyererei and Pundamilia pundamilia

This study compared Pundamilia nyererei and Pundamilia pundamilia males in routine metabolic rate (R_R) and in the metabolic costs males pay during territorial interactions (active metabolic rate, R_A). Pundamilia nyererei and P. pundamilia males housed in social isolation did not differ in R_R. In contrast to expectation, however, P. nyererei males used less oxygen than P. pundamilia males, for a given mass and level of agonistic activity. This increased metabolic efficiency may be an adaptation to limit the metabolic cost that P. nyererei males pay for their higher rate of aggressiveness compared to P. pundamilia males. Thus, the divergence between the species in agonistic behaviour is correlated with metabolic differentiation. Such concerted divergence in physiology and behaviour might be widespread in the dramatically diverse cichlid radiations in East African lakes and may be an important factor in the remarkably rapid speciation of these fishes. The results did not support the hypothesis that higher metabolic rates caused a physiological cost to P. nyererei males that would offset their dominance advantage.     

A quantitative genetic competition model for sympatric speciation

I use multilocus genetics to describe assortative mating in a competition model. The intensity of competition between individuals is influenced by a quantitative character whose value is determined additively by alleles from many loci. With assortative mating based on this character, frequency- and density-dependent competition can subdivide a population with an initially unimodal character distribution. The character distribution becomes bimodal, and the subpopulations corresponding to the two modes are reproductively separated because mating is assortative. This happens if the resource distribution is unimodal, i.e. even if selection due to phenotypic carrying capacities is not disruptive. The results suggest that sympatric speciation due to frequency-dependent selection can occur in quite general ecological scenarios if mating is assortative. I also discuss the evolution of assortative mating. Since it induces bimodal phenotype distributions, assortative mating leads to a better match of the resources if their distribution is also bimodal. Moreover, in a population with a bimodal phenotype distribution, the average strength of frequency-dependent competition is lower than in a unimodal population. Therefore, assortative mating permits higher equilibrium densities than random mating even if the resource distribution is unimodal. Thus, even though it may lead to a less efficient resource use, assortative mating is favoured over random mating because it reduces frequency-dependent effects of competition.     

Mixed responses to resource densities and their implications for character displacement

Summary How should a consumer of two resource types adapt to changes in their abundances? This paper shows that many different biological circumstances produce mixed responses; i.e. increasing availability of one resource increases the consumer's efforts to obtain it, while increasing availability of the other resource decreases the consumer's efforts at exploitation. This implies that competition from a second consumer species may cause convergent or divergent character displacement of the first species. The signs and magnitudes of the second derivative of the fitness function are important in determining which outcome occurs. The degree of resource limitation of the consumer species also influences the nature of adaptive shifts in resource use.     

Genetics of male nuptial colour divergence between sympatric sister species of a Lake Victoria cichlid fish

The hypothesis of sympatric speciation by sexual selection has been contentious. Several recent theoretical models of sympatric speciation by disruptive sexual selection were tailored to apply to African cichlids. Most of this work concludes that the genetic architecture of female preference and male trait is a key determinant of the likelihood of disruptive sexual selection to result in speciation. We investigated the genetic architecture controlling male nuptial colouration in a sympatric sibling species pair of cichlid fish from Lake Victoria, which differ conspicuously in male colouration and female mating preferences for these. We estimated that the difference between the species in male nuptial red colouration is controlled by a minimum number of two to four genes with significant epistasis and dominance effects. Yellow colouration appears to be controlled by one gene with complete dominance. The two colours appear to be epistatically linked. Knowledge on how male colouration segregates in hybrid generations and on the number of genes controlling differences between species can help us assess whether assumptions made in simulation models of sympatric speciation by sexual selection are realistic. In the particular case of the two sister species that we studied a small number of genes causing major differences in male colouration may have facilitated the divergence in male colouration associated with speciation.     

Ecological divergence associated with mating system causes nearly complete reproductive isolation between sympatric Mimulus species

Speciation often involves the evolution of numerous prezygotic and postzygotic isolating barriers between divergent populations. Detailed knowledge of the strength and nature of those barriers provides insight into ecological and genetic factors that directly or indirectly influenced their origin, and may help predict whether they will be maintained in the face of sympatric hybridization and introgression. We estimated the magnitude of pre- and postzygotic barriers between naturally occurring sympatric populations of Mimulus guttatus and M. nasutus. Prezygotic barriers, including divergent flowering phenologies, differential pollen production, mating system isolation, and conspecific pollen precedence, act asymmetrically to completely prevent the formation of F(1) hybrids among seeds produced by M. guttatus (F(1)g), and reduce F(1) hybrid production among seeds produced by M. nasutus (F(1)n) to only about 1%. Postzygotic isolation is also asymmetric: in field experiments, F(1)g but not F(1)n hybrids had significantly reduced germination rates and survivorship compared to parental species. Both hybrid classes had flower, pollen, and seed production values within the range of parental values. Despite the moderate degree of F(1)g hybrid inviability, postzygotic isolation contributes very little to the total isolation between these species in the wild. We also found that F(1) hybrid flowering phenology overlapped more with M. guttatus than M. nasutus. These results, taken together, suggest greater potential for introgression from M. nasutus to M. guttatus than for the reverse direction. We also address problems with commonly used indices of isolation, discuss difficulties in calculating meaningful measures of reproductive isolation when barriers are asymmetric, and propose novel measures of prezygotic isolation that are consistent with postzygotic measures.     

Prominent intraspecific genetic divergence within Anopheles gambiae sibling species triggered by habitat discontinuities across a riverine landscape

The Anopheles gambiae complex of mosquitoes includes malaria vectors at different stages of speciation, whose study enables a better understanding of how adaptation to divergent environmental conditions leads to evolution of reproductive isolation. We investigated the population genetic structure of closely related sympatric taxa that have recently been proposed as separate species (An. coluzzii and An. gambiae), sampled from diverse habitats along the Gambia river in West Africa. We characterized putatively neutral microsatellite loci as well as chromosomal inversion polymorphisms known to be associated with ecological adaptation. The results revealed strong ecologically associated population subdivisions within both species. Microsatellite loci on chromosome‐3L revealed clear differentiation between coastal and inland populations, which in An. coluzzii is reinforced by a unusual inversion polymorphism pattern, supporting the hypothesis of genetic divergence driven by adaptation to the coastal habitat. A strong reduction of gene flow was observed between An. gambiae populations west and east of an extensively rice‐cultivated region apparently colonized exclusively by An. coluzzii. Notably, this ‘intraspecific’ differentiation is higher than that observed between the two species and involves also the centromeric region of chromosome‐X which has previously been considered a marker of speciation within this complex, possibly suggesting that the two populations may be at an advanced stage of differentiation triggered by human‐made habitat fragmentation. These results confirm ongoing ecological speciation within these most important Afro‐tropical malaria vectors and raise new questions on the possible effect of this process in malaria transmission.     

Low intraspecific variation for genomic isolation between hybridizing sunflower species

Barriers to gene flow between species result from selection against foreign linkage blocks in hybrids. When the geographic ranges of taxa meet at multiple locations, the opportunity exists for variation in the genetic architecture of isolating barriers. Hybrid zones between two sunflower species (Helianthus annuus and H. petiolaris) in Nebraska and California exhibited remarkably similar patterns of introgression of mapped molecular markers. Congruence among hybrid zones may result from limited intraspecific variation at loci contributing to isolation and from similar selective effects of alleles in the heterospecific genetic background. The observed consistency of introgression patterns across distantly separated hybrid zones suggests that intrinsic forces predominate in determining hybrid zone dynamics and boundaries between these sunflower species.     

Sexual selection and population divergence III: Interspecific and intraspecific variation in mating signals

A major challenge for studying the role of sexual selection in divergence and speciation is understanding the relative influence of different sexually selected signals on those processes in both intra‐ and interspecific contexts. Different signals may be more or less susceptible to co‐option for species identification depending on the balance of sexual and ecological selection acting upon them. To examine this, we tested three predictions to explain geographic variation in long‐ versus short‐range sexual signals across a 3,500 + km transect of two related Australian field cricket species (Teleogryllus spp.): (a) selection for species recognition, (b) environmental adaptation and (c) stochastic divergence. We measured male calling song and male and female cuticular hydrocarbons (CHCs) in offspring derived from wild populations, reared under common garden conditions. Song clearly differentiated the species, and no hybrids were observed suggesting that hybridization is rare or absent. Spatial variation in song was not predicted by geography, genetics or climatic factors in either species. In contrast, CHC divergence was strongly associated with an environmental gradient supporting the idea that the climatic environment selects more directly upon these chemical signals. In light of recently advocated models of diversification via ecological selection on secondary sexual traits, the different environmental associations we found for song and CHCs suggest that the impact of ecological selection on population divergence, and how that influences speciation, might be different for acoustic versus chemical signals.