Kjetil L. Voje

Evolution of morphological allometry

Morphological allometry refers to patterns of covariance between body parts resulting from variation in body size. Whether measured during growth (ontogenetic allometry), among individuals at similar developmental stage (static allometry), or among populations or species (evolutionary allometry), allometric relationships are often tight and relatively invariant. Consequently, it has been suggested that allometries have low evolvability and could constrain phenotypic evolution by forcing evolving species along fixed trajectories. Alternatively, allometric relationships may result from natural selection for functional optimization. Despite nearly a century of active research, distinguishing between these alternatives remains difficult, partly due to wide differences in the meaning assigned to the term allometry. In particular, a broad use of the term, encompassing any monotonic relationship between body parts, has become common. This usage breaks the connection to the proportional growth regulation that motivated Huxleys original narrow‐sense use of allometry to refer to power–law relationships between traits. Focusing on the narrow‐sense definition of allometry, we review here evidence for and against the allometry‐as‐a‐constraint hypothesis. Although the low evolvability and the evolutionary invariance of the static allometric slope observed in some studies suggest a possible constraining effect of this parameter on phenotypic evolution, the lack of knowledge about selection on allometry prevents firm conclusions.

ALLOMETRIC CONSTRAINTS AND THE EVOLUTION OF ALLOMETRY

Morphological traits often covary within and among species according to simple power laws referred to as allometry. Such allometric relationships may result from common growth regulation, and this has given rise to the hypothesis that allometric exponents may have low evolvability and constrain trait evolution. We formalize hypotheses for how allometry may constrain morphological trait evolution across taxa, and test these using more than 300 empirical estimates of static (within‐species) allometric relations of animal morphological traits. Although we find evidence for evolutionary changes in allometric parameters on million‐year, cross‐species time scales, there is limited evidence for microevolutionary changes in allometric slopes. Accordingly, we find that static allometries often predict evolutionary allometries on the subspecies level, but less so across species. Although there is a large body of work on allometry in a broad sense that includes all kinds of morphological trait–size relationships, we found relatively little information about the evolution of allometry in the narrow sense of a power relationship. Despite the many claims of microevolutionary changes of static allometries in the literature, hardly any of these apply to narrow‐sense allometry, and we argue that the hypothesis of strongly constrained static allometric slopes remains viable.

Hybrid speciation in sparrows II: a role for sex chromosomes?

Homoploid hybrid speciation in animals is poorly understood, mainly because of the scarcity of well‐documented cases. Here, we present the results of a multilocus sequence analysis on the house sparrow (Passer domesticus), Spanish sparrow (P. hispaniolensis) and their proposed hybrid descendant, the Italian sparrow (P. italiae). The Italian sparrow is shown to be genetically intermediate between the house sparrow and Spanish sparrow, exhibiting genealogical discordance and a mosaic pattern of alleles derived from either of the putative parental species. The average variation on the Z chromosome was significantly reduced compared with autosomal variation in the putative parental species, the house sparrow and Spanish sparrow. Additionally, divergence between the two species was elevated on the Z chromosome relative to the autosomes. This pattern of variation and divergence is consistent with reduced introgression of Z‐linked genes and/or a faster‐Z effect (increased rate of adaptive divergence on the Z). FST‐outlier tests were consistent with the faster‐Z hypothesis: two of five Z‐linked loci (CHD1Z and PLAA) were identified as candidates for being subject to positive, divergent selection in the putative parental species. Interestingly, the two latter genes showed a mosaic pattern in the (hybrid) Italian sparrow; that is, the Italian sparrow was found to be fixed for Spanish sparrow alleles at CHD1Z and to mainly have house sparrow alleles at PLAA. Preliminary evidence presented in this study thus suggests that sex chromosomes may play a significant role in this case of homoploid hybrid speciation.

Climatic change as an engine for speciation in flightless Orthoptera species inhabiting African mountains

Many East African mountains are characterized by an exceptionally high biodiversity. Here we assess the hypothesis that climatic fluctuations during the Plio‐Pleistocene led to ecological fragmentation with subsequent genetic isolation and speciation in forest habitats in East Africa. Hypotheses on speciation in savannah lineages are also investigated. To do this, mitochondrial DNA sequences from a group of bush crickets consisting of both forest and savannah inhabiting taxa were analysed in relation to Plio‐Pleistocene range fragmentations indicated by palaeoclimatic studies. Coalescent modelling and mismatch distributions were used to distinguish between alternative biogeographical scenarios. The results indicate two radiations: the earliest one overlaps in time with the global spread of C4 grasslands and only grassland inhabiting lineages originated in this radiation. Climatically induced retraction of forest to higher altitudes about 0.8 million years ago, promoting vicariant speciation in species inhabiting the montane zone, can explain the second radiation. Although much of the biodiversity in East Africa is presently threatened by climate change, past climatic fluctuations appear to have contributed to the species richness observed in the East African hot spots. Perceiving forests as centres of speciation reinforces the importance of conserving the remaining forest patches in the region.

Evolution of static allometries: adaptive change in allometric slopes of eye span in stalk-eyed flies.

Julian Huxley showed that within‐species (static) allometric (power‐law) relations can arise from proportional growth regulation with the exponent in the power law equaling the factor of proportionality. Allometric exponents may therefore be hard to change and act as constraints on the independent evolution of traits. In apparent contradiction to this, many empirical studies have concluded that static allometries are evolvable. Many of these studies have been based, however, on a broad definition of allometry that includes any monotonic shape change with size, and do not falsify the hypothesis of constrained narrow‐sense allometry. Here, we present the first phylogenetic comparative study of narrow‐sense allometric exponents based on a reanalysis of data on eye span and body size in stalk‐eyed flies (Diopsidae). Consistent with a role in sexual selection, we found strong evidence that male slopes were tracking “optima” based on sexual dimorphism and relative male trait size. This tracking was slow, however, with estimated times of 2–3 million years for adaptation to exceed ancestral influence on the trait. Our results are therefore consistent with adaptive evolution on million‐year time scales, but cannot rule out that static allometry may act as a constraint on eye‐span adaptation at shorter time scales.

The role of biotic forces in driving macroevolution: beyond the Red Queen.

A multitude of hypotheses claim that abiotic factors are the main drivers of macroevolutionary change. By contrast, Van Valens Red Queen hypothesis is often put forward as the sole representative of the view that biotic forcing is the main evolutionary driver. This imbalance of hypotheses does not reflect our current knowledge: theoretical work demonstrates the plausibility of biotically driven long-term evolution, whereas empirical work suggests a central role for biotic forcing in macroevolution. We call for a more pluralistic view of how biotic forces may drive long-term evolution that is compatible with both phenotypic stasis in the fossil record and with non-constant extinction rates. Promising avenues of research include contrasting predictions from relevant theories within ecology and macroevolution, as well as embracing both abiotic and biotic proxies while modelling long-term evolutionary data. By fitting models describing hypotheses of biotically driven macroevolution to data, we could dissect their predictions and transcend beyond pattern description, possibly narrowing the divide between our current understanding of micro- and macroevolution.

Selection and inertia in the evolution of holocentric chromosomes in sedges (Carex, Cyperaceae)

• Changes in chromosome number as a result of fission and fusion in holocentrics have direct and immediate effects on the recombination rate. We investigate the support for the classic hypothesis that environmental stability selects for increased recombination rates. • We employed a phylogenetic and cytogenetic data set from one of the most diverse angiosperm genera in the world, which has the largest nonpolyploid chromosome radiation (Carex, Cyperaceae; 2n = 12-124; 2100 spp.). We evaluated alternative Ornstein-Uhlenbeck models of chromosome number adaptation to the environment in an information-theoretic framework. • We found moderate support for a positive influence of lateral inflorescence unit size on chromosome number, which may be selected in a stable environment in which resources for reproductive investment are larger. We found weak support for a positive influence on chromosome number of water-saturated soils and among-month temperature constancy, which would be expected to be negatively select for pioneering species. Chromosome number showed a strong phylogenetic signal. • We argue that our finding of small but significant effects of life history and ecology is compatible with our original hypothesis regarding selection of optima in recombination rates: low recombination rate is optimal when inmediate fitness is required. By contrast, high recombination rate is optimal when stable environments allow for evolutionary innovation.

Deviation from the line of least resistance does not exclude genetic constraints: a comment on Berner et al. (2010).

Berner et al. (2010) found that freshwater adaptation of three‐spined sticklebacks had not followed the direction of maximal evolvability. Based on this, they suggested that ancestral variance structure has not appreciably biased adaptive diversification. We reanalyze their data to show that evolution has happened in directions of much larger than average evolvability, and we conclude that their data are consistent with an influence of ancestral variational constraints.

Adaptation and constraint in a stickleback radiation

The evolution of threespine sticklebacks in freshwater lakes constitutes a well‐studied example of a phenotypic radiation that has produced numerous instances of parallel evolution, but the exact selective agents that drive these changes are not yet fully understood. We present a comparative study across 74 freshwater populations of threespine stickleback in Norway to test whether evolutionary changes in stickleback morphology are consistent with adaptations to physical parameters such as lake depth, lake area, lake perimeter and shoreline complexity, variables thought to reflect different habitats and feeding niches. Only weak indications of adaptation were found. Instead, populations seem to have diversified in phenotypic directions consistent with allometric scaling relationships. This indicates that evolutionary constraints may have played a role in structuring phenotypic variation across freshwater populations of stickleback. We also tested whether the number of lateral plates evolved in response to lake calcium levels, but found no evidence for this hypothesis.

Scaling of Morphological Characters across Trait Type, Sex, and Environment

Biological diversity is, to a large extent, a matter of variation in size. Proportional (isometric) scaling, where large and small individuals are magnified versions of each other, is often assumed to be the most common way morphological traits scale relative to overall size within species. However, the many traits showing nonproportional (allometric) scaling have motivated some of the most discussed hypotheses on scaling relationships in biology, like the positive allometry hypothesis for secondary sexual traits and the negative allometry hypothesis for genitals. I evaluate more than 3,200 allometric parameters from the literature and find that negative allometry, not isometry, is the expected scaling relationship of morphological traits within species. Slopes of secondary sexual traits are more often steeper compared with other traits, but slopes larger than unity are also common for traits not under sexual selection. The steepness of the allometric slope is accordingly a weak predictor of past and present patterns of selection. Scaling of genitals varies across taxonomic groups, but negative allometry of genitals in insects and spiders is a consistent pattern. Finally, I find indications that terrestrial organisms may have a different scaling of morphological traits overall compared with aquatic species.