Matthew D. McGee

Genetics of ecological divergence during speciation

Ecological differences often evolve early in speciation as divergent natural selection drives adaptation to distinct ecological niches, leading ultimately to reproductive isolation. Although this process is a major generator of biodiversity, its genetic basis is still poorly understood. Here we investigate the genetic architecture of niche differentiation in a sympatric species pair of threespine stickleback fish by mapping the environment-dependent effects of phenotypic traits on hybrid feeding and performance under semi-natural conditions. We show that multiple, unlinked loci act largely additively to determine position along the major niche axis separating these recently diverged species. We also find that functional mismatch between phenotypic traits reduces the growth of some stickleback hybrids beyond that expected from an intermediate phenotype, suggesting a role for epistasis between the underlying genes. This functional mismatch might lead to hybrid incompatibilities that are analogous to those underlying intrinsic reproductive isolation but depend on the ecological context.

Resource polyphenism increases species richness: a test of the hypothesis

A major goal of evolutionary biology is to identify the causes of diversification and to ascertain why some evolutionary lineages are especially diverse. Evolutionary biologists have long speculated that polyphenism—where a single genome produces alternative phenotypes in response to different environmental stimuli—facilitates speciation, especially when these alternative phenotypes differ in resource or habitat use, i.e. resource polyphenism. Here, we present a series of replicated sister-group comparisons showing that fishes and amphibian clades in which resource polyphenism has evolved are more species rich, and have broader geographical ranges, than closely related clades lacking resource polyphenism. Resource polyphenism may promote diversification by facilitating each of the different stages of the speciation process (isolation, divergence, reproductive isolation) and/or by reducing a lineages risk of extinction. Generally, resource polyphenism may play a key role in fostering diversity, and species in which resource polyphenism has evolved may be predisposed to diversify.

Functional basis of ecological divergence in sympatric stickleback

BackgroundThe evolution of ecological divergence in closely related species is a key component of adaptive radiation. However, in most examples of adaptive radiation the mechanistic basis of ecological divergence remains unclear. A classic example is seen in the young benthic and limnetic stickleback species pairs of British Columbia. In each pair the benthic species feeds on littoral macroinvertebrates whereas the limnetic feeds on pelagic zooplankton. Previous studies indicate that in both short-term feeding trials and long-term enclosure studies, benthics and limnetics exhibit enhanced performance on their own resource but fare more poorly on the other species’ resource. We examined the functional basis of ecological divergence in the stickleback species pair from Paxton Lake, BC, using biomechanical models of fish feeding applied to morphological traits. We examined the consequences of morphological differences using high speed video of feeding fish.ResultsBenthic stickleback possess morphological traits that predict high suction generation capacity, including greatly hypertrophied epaxial musculature. In contrast, limnetic stickleback possess traits thought to enhance capture of evasive planktonic prey, including greater jaw protrusion than benthics and greater displacement advantage in both the lower jaw-opening lever system and the opercular four-bar linkage. Kinematic data support the expectations from the morphological analysis that limnetic stickleback exhibit faster strikes and greater jaw protrusion than benthic fish, whereas benthics exert greater suction force on attached prey.ConclusionsWe reveal a previously unknown suite of complex morphological traits that affect rapid ecological divergence in sympatric stickleback. These results indicate that postglacial divergence in stickleback involves many functional systems and shows the value of investigating the functional consequences of phenotypic divergence in adaptive radiation.

CONVERGENT EVOLUTION AS A GENERATOR OF PHENOTYPIC DIVERSITY IN THREESPINE STICKLEBACK

Convergent evolution, in which populations produce similar phenotypes in response to similar selection pressure, is strong evidence for the role of natural selection in shaping biological diversity. In some cases, closely related populations can produce functionally similar but phenotypically divergence forms in response to selection. Functional convergence with morphological divergence has been observed in laboratory selection experiments and computer simulations, but while potentially common, is rarely recognized in nature. Here, we present data from the North Pacific threespine stickleback radiation showing that ecologically and functionally similar, but morphologically divergent phenotypes rapidly evolved when an ancestral population colonized freshwater benthic habitats in parallel. In addition, we show that in this system, functional convergence substantially increases morphospace occupation relative to ancestral phenotypes, which suggests that convergent evolution may, paradoxically, be an important and previously underappreciated source of morphological diversity.

Origins, Innovations, and Diversification of Suction Feeding in Vertebrates

We review the origins, prominent innovations, and major patterns of diversification in suction feeding by vertebrates. Non-vertebrate chordates and larval lamprey suspension-feed by capturing small particles in pharyngeal mucous. In most of these lineages the gentle flows that transport particles are generated by buccal cilia, although larval lamprey and thaliacean urochordates have independently evolved a weak buccal pump to generate an oscillating flow of water that is powered by elastic recovery of the pharynx following compression by buccal muscles. The evolution of jaws and the hyoid facilitated powerful buccal expansion and high-performance suction feeding as found today throughout aquatic vertebrates. We highlight three major innovations in suction feeding. Most vertebrate suction feeders have mechanisms that occlude the corners of the open mouth during feeding. This produces a planar opening that is often nearly circular in shape. Both features contribute to efficient flow of water into the mouth and help direct the flow to the area directly in front of the mouths aperture. Among several functions that have been identified for protrusion of the upper jaw, is an increase in the hydrodynamic forces that suction feeders exert on their prey. Protrusion of the upper jaw has evolved five times in ray-finned fishes, including in two of the most successful teleost radiations, cypriniforms and acanthomorphs, and is found in about 60% of living teleost species. Diversification of the mechanisms of suction feeding and of feeding behavior reveals that suction feeders with high capacity for suction rarely approach their prey rapidly, while slender-bodied predators with low capacity for suction show the full range of attack speeds. We hypothesize that a dominant axis of diversification among suction feeders involves a trade-off between the forces that are exerted on prey and the volume of water that is ingested.

A pharyngeal jaw evolutionary innovation facilitated extinction in Lake Victoria cichlids

The downside of innovation Evolutionary innovation allows a species to invade a new niche or environment. Generally, the emergence of adaptive traits is thought to lead to diversification. Support for this process in nature, however, is mixed. McGee et al. show that the evolution of secondary jaws in fish may be an example of how innovation can reduce diversification (see the Perspective by Vermeij). Fish with secondary jaws are less able to rapidly ingest fish prey, which puts them at a competitive disadvantage to regularly jawed fish. Such competition could lead to reduced variation and the extinction of lineages with the trait. Science, this issue p. 1077; see also p. 1038 Jaw specialization in fish may have paradoxically reduced speciation in the African Great Lakes. [Also see Perspective by Vermeij] Evolutionary innovations, traits that give species access to previously unoccupied niches, may promote speciation and adaptive radiation. Here, we show that such innovations can also result in competitive inferiority and extinction. We present evidence that the modified pharyngeal jaws of cichlid fishes and several marine fish lineages, a classic example of evolutionary innovation, are not universally beneficial. A large-scale analysis of dietary evolution across marine fish lineages reveals that the innovation compromises access to energy-rich predator niches. We show that this competitive inferiority shaped the adaptive radiation of cichlids in Lake Tanganyika and played a pivotal and previously unrecognized role in the mass extinction of cichlid fishes in Lake Victoria after Nile perch invasion.

Replicated divergence in cichlid radiations mirrors a major vertebrate innovation

Decoupling of the upper jaw bones—jaw kinesis—is a distinctive feature of the ray-finned fishes, but it is not clear how the innovation is related to the extraordinary diversity of feeding behaviours and feeding ecology in this group. We address this issue in a lineage of ray-finned fishes that is well known for its ecological and functional diversity—African rift lake cichlids. We sequenced ultraconserved elements to generate a phylogenomic tree of the Lake Tanganyika and Lake Malawi cichlid radiations. We filmed a diverse array of over 50 cichlid species capturing live prey and quantified the extent of jaw kinesis in the premaxillary and maxillary bones. Our combination of phylogenomic and kinematic data reveals a strong association between biting modes of feeding and reduced jaw kinesis, suggesting that the contrasting demands of biting and suction feeding have strongly influenced cranial evolution in both cichlid radiations.

Evaluating genomic divergence and parallelism in replicate ecomorphs from young and old cichlid adaptive radiations

Comparative genomic studies of closely related species typically focus on single species pairs at one given stage of divergence. That makes it difficult to infer the continuum of evolutionary process during speciation and beyond. Here, we use whole‐genome resequencing to examine genomic patterns of divergence in three sympatric cichlid species pairs with very similar functional and ecological differentiation, but different ages. We find a strong signature of increasing genomic divergence with time in both the mitochondrial genome and the nuclear genome. In contrast to many other systems, we find that in these cichlids, regions of elevated relative differentiation also exhibit increased absolute differentiation. We detect a signature of convergent evolution in a comparison of outlier regions across all three species pair comparisons, but the extent of it is modest, and regions that are strongly divergent in any one pair tend to be only slightly elevated in the other pairs, consistent with a repeatable but polygenic basis of traits that characterize the ecomorphs. Our results suggest that strong functional phenotypic differentiation, as seen in all three species pairs, is generally associated with a clear signature of genomic divergence, even in the youngest species pair.

Body ram, not suction, is the primary axis of suction feeding diversity in spiny-rayed fishes

ABSTRACT Suction-feeding fishes exhibit diverse prey-capture strategies that vary in their relative use of suction and predator approach (ram), which is often referred to as the ram–suction continuum. Previous research has found that ram varies more than suction distance among species, such that ram accounts for most differences in prey-capture behaviors. To determine whether these findings hold at broad evolutionary scales, we collected high-speed videos of 40 species of spiny-rayed fishes (Acanthomorpha) feeding on live prey. For each strike, we calculated the contributions of suction, body ram (swimming) and jaw ram (mouth movement relative to the body) to closing the distance between predator and prey. We confirm that the contribution of suction distance is limited even in this phylogenetically and ecologically broad sample of species, with the extreme suction area of prey-capture space conspicuously unoccupied. Instead of a continuum from suction to ram, we find that variation in body ram is the major factor underlying the diversity of prey-capture strategies among suction-feeding fishes. Independent measurement of the contribution of jaw ram revealed that it is an important component of diversity among spiny-rayed fishes, with a number of ecomorphologies relying heavily on jaw ram, including pivot feeding in syngnathiforms, extreme jaw protruders and benthic sit-and-wait ambush predators. A combination of morphological and behavioral innovations has allowed fish to invade the extreme jaw ram area of prey-capture space. We caution that while two-species comparisons may support a ram–suction trade-off, these patterns do not speak to broader patterns across spiny-rayed fishes. Summary: Acanthomorph fishes exhibit a large diversity of suction-feeding behaviors, which is driven by variation in the contribution of body ram. Suction distances are constrained even at broad evolutionary scales.

Intermediate Kinematics Produce Inferior Feeding Performance in a Classic Case of Natural Hybridization

Selection on naturally occurring hybrid individuals is a key component of speciation theory, but few studies examine the functional basis of hybrid performance. We examine the functional consequences of hybridization in nature, using the freshwater sunfishes (Centrarchidae), where natural hybrids have been studied for more than a century and a half. We examined bluegill (Lepomis macrochirus), green sunfish (Lepomis cyanellus), and their naturally occurring hybrid, using prey-capture kinematics and morphology to parameterize suction-feeding simulations on divergent parental resources. Hybrid individuals exhibited kinematics intermediate between those of the two parental species. However, performance assays indicated that hybrids display performance most similar to the worse-performing species for a given parental resource. Our results show that intermediate hybrid phenotypes can be impaired by a less-than-intermediate performance and hence suffer a larger loss in fitness than could be inferred from morphology alone.