Analytical advances alleviate model misspecification in non-Brownian multivariate comparative methods.

Adams and Collyer argue that contemporary multivariate (Gaussian) phylogenetic comparative methods are prone to favouring more complex models of evolution and sometimes rotation invariance can be an issue. Here we dissect the concept of rotation invariance and point out that, depending on the understanding, this can be an issue with any method that relies on numerical instead of analytical estimation approaches. We relate this to the ongoing discussion concerning phylogenetic principal component analysis. Contrary to what Adams and Collyer found, we do not observe a bias against the simpler Brownian motion process in simulations when we use the new, improved, likelihood evaluation algorithm employed by mvSLOUCH, which allows for studying much larger phylogenies and more complex model setups.

Fitting and evaluating univariate and multivariate models of within-lineage evolution.

The nature of phenotypic evolution within lineages is central to many unresolved questions in paleontology and evolutionary biology. Analyses of evolutionary time-series of ancestor-descendant populations in the fossil record are likely to make important contributions to many of these debates. However, the limited number of models that have been applied to these types of data may restrict our ability to interpret phenotypic evolution in the fossil record. Using uni- and multivariate models of trait evolution that make different assumptions regarding the dynamics of the adaptive landscape, I evaluate contrasting hypotheses to explain evolution of size in the radiolarian Eucyrtidium calvertense and armor in the stickleback Gaserosteus doryssus. Body size evolution in E. calvertense is best explained by a model where the lineage evolves as a consequence of a shift in the adaptive landscape that coincides with the initiation of neosympatry with its sister lineage. Multivariate evolution of armor traits in a stickleback lineage (Gasterosteus doryssus) show evidence of adaptation towards independent optima on the adaptive landscape at the same time as traits change in a correlated fashion. The fitted models are available in a the R package evoTS, which builds on the commonly used paleoTS framework.

Measurement theory and paleobiology.

Measurement theory, a branch of applied mathematics, offers guiding principles for extracting meaning from empirical observations and is applicable to any science involving measurements. Measurement theory is highly relevant in paleobiology because statistical approaches assuming ratio-scaled variables are commonly used on data belonging to nominal and ordinal scale types. We provide an informal introduction to representational measurement theory and argue for its importance in robust scientific inquiry. Although measurement theory is widely applicable in paleobiology research, we use the study of disparity to illustrate measurement theoretical challenges in the quantitative study of the fossil record. Respecting the inherent properties of different measurements enables meaningful inferences about evolutionary and ecological processes from paleontological data.

Model Selection Performance in Phylogenetic Comparative Methods Under Multivariate Ornstein-Uhlenbeck Models of Trait Evolution.

The advent of fast computational algorithms for phylogenetic comparative methods allows for considering multiple hypotheses concerning the co-adaptation of traits and also for studying if it is possible to distinguish between such models based on contemporary species measurements. Here we demonstrate how one can perform a study with multiple competing hypotheses using mvSLOUCH by analyzing two data sets, one concerning feeding styles and oral morphology in ungulates, and the other concerning fruit evolution in Ferula (Apiaceae). We also perform simulations to determine if it is possible to distinguish between various adaptive hypotheses. We find that Akaike's information criterion corrected for small sample size has the ability to distinguish between most pairs of considered models. However, in some cases there seems to be bias towards Brownian motion or simpler Ornstein-Uhlenbeck models. We also find that measurement error and forcing the sign of the diagonal of the drift matrix for an Ornstein-Uhlenbeck process influences identifiability capabilities. It is a cliché that some models, despite being imperfect, are more useful than others. Nonetheless, having a much larger repertoire of models will surely lead to a better understanding of the natural world, as it will allow for dissecting in what ways they are wrong. [Adaptation; AICc; model selection; multivariate Ornstein-Uhlenbeck process; multivariate phylogenetic comparative methods; mvSLOUCH.].

Revisiting a Landmark Study System: No Evidence for a Punctuated Mode of Evolution in Metrarabdotos.

Is speciation generally a "special time" in morphological evolution, or are lineage-splitting events just "more of the same" where the end product happens to be two separate lineages? Data on evolutionary dynamics during anagenetic and cladogenetic events among closely related lineages within a clade are rare, but the fossil record of the bryozoan genus Metrarabdotos is considered a textbook example of a clade where speciation causes rapid evolutionary change against a backdrop of morphological stasis within lineages. Here, we point to some methodological and measurement theoretical issues in the original work on Metrarabdotos. We then reanalyze a subset of the original data that can be meaningfully investigated using quantitative statistical approaches similar to those used in the original studies. We consistently fail to find variation in the evolutionary process during within-lineage evolution compared with cladogenetic events: the rates of evolution, the strength of selection, and the directions traveled in multivariate morphospace are not different when comparing evolution within lineages and at speciation events in Metrarabdotos, and genetic drift cannot be excluded as a sufficient explanation for the morphological differentiation within lineages and during speciation. Although widely considered the best example of a punctuated mode of evolution, morphological divergence and speciation are not linked in Metrarabdotos.

Testing eco-evolutionary predictions using fossil data: Phyletic evolution following ecological opportunity.

Fossil sequences provide observations of phenotypes within a lineage over time and represent essential data for increasing our understanding of phyletic evolution beyond microevolutionary timescales. I investigate if fossil time series of the diatom Stephanodiscus niagarae/yellowstonensis follow evolutionary dynamics compatible with hypotheses for how the adaptive landscape changes when a population enters a new environment. The lineage-which has a remarkably detailed stratigraphic record-invaded Yellowstone Lake immediately after recession of ice from the basin 14,000 years ago. Several phyletic models portraying different types of evolutionary dynamics-both compatible and not compatible with changes in the adaptive landscape following ecological opportunity-were fitted to the fossil times-series of S. niagarae/yellowstonensis. Different models best describe the three analyzed traits. Two of the models (a new model of decelerated evolution and an Ornstein-Uhlenbeck model) capture trait dynamics compatible with an event of ecological opportunity, whereas the third model (random walk) does not. Entering a new environment may accordingly affect trait dynamics for thousands of years, but the effects can vary across phenotypes. However, tests of model adequacy reveal shortcomings in all three models explaining the trait dynamics, suggesting model development is needed to more fully understand the phyletic evolution in S. niagarae/yellowstonensis.

Model Adequacy and Microevolutionary Explanations for Stasis in the Fossil Record.

Long-term phenotypic stasis is frequently observed in the fossil record, but not readily predicted from microevolutionary theory. To test competing explanations for stasis on macroevolutionary timescales we need reliably estimated parameters from appropriate evolutionary models that adequately describe the evolutionary trait dynamics. Here, we develop tests to assess the adequacy of the most commonly used stasis model in evolutionary biology and apply them to time series of phenotypic traits from fossil lineages. Of the 572 fossil time series we analyzed from the literature, 263 time series showed a better fit to the stasis model relative to alternative models, but only 172 of those fitted the stasis model in both relative and absolute terms. The estimated trait variances from these 172 time series do not correlate with rough proxies of effective population size. Our preliminary investigation of the fixed-optimum hypothesis hence fails to give empirical support to the idea that genetic drift around a constant trait optimum is an explanation for stasis in the fossil record. We argue that optima following stationary processes on the adaptive landscape is a viable hypothesis for stasis that needs further investigation. We end by discussing how investigations of model adequacy can be a valuable approach for increasing our understanding of the dynamics of the adaptive landscape on macroevolutionary timescales.

Evolution of Hemoglobin Genes in Codfishes Influenced by Ocean Depth.

Understanding the genetic basis of adaptation is one of the main enigmas of evolutionary biology. Among vertebrates, hemoglobin has been well documented as a key trait for adaptation to different environments. Here, we investigate the role of hemoglobins in adaptation to ocean depth in the diverse teleost order Gadiformes, with species distributed at a wide range of depths varying in temperature, hydrostatic pressure and oxygen levels. Using genomic data we characterized the full hemoglobin (Hb) gene repertoire for subset of species within this lineage. We discovered a correlation between expanded numbers of Hb genes and ocean depth, with the highest numbers in species occupying shallower, epipelagic regions. Moreover, we demonstrate that the Hb genes have functionally diverged through diversifying selection. Our results suggest that the more variable environment in shallower water has led to selection for a larger Hb gene repertoire and that Hbs have a key role in adaptive processes in marine environments.

Linking species habitat and past palaeoclimatic events to evolution of the teleost innate immune system.

Host-intrinsic factors as well as environmental changes are known to be strong evolutionary drivers defining the genetic foundation of immunity. Using a novel set of teleost genomes and a time-calibrated phylogeny, we here investigate the family of Toll-like receptor (TLR) genes and address the underlying evolutionary processes shaping the diversity of the first-line defence. Our findings reveal remarkable flexibility within the evolutionary design of teleost innate immunity characterized by prominent TLR gene losses and expansions. In the order of Gadiformes, expansions correlate with the loss of major histocompatibility complex class II (MHCII) and diversifying selection analyses support that this has fostered new immunological innovations in TLRs within this lineage. In teleosts overall, TLRs expansions correlate with species latitudinal distributions and maximum depth. By contrast, lineage-specific gene losses overlap with well-described changes in palaeoclimate (global ocean anoxia) and past Atlantic Ocean geography. In conclusion, we suggest that the evolvability of the teleost immune system has most likely played a prominent role in the survival and successful radiation of this lineage.

Rapid adaptive phenotypic change following colonization of a newly restored habitat.

Real-time observation of adaptive evolution in the wild is rare and limited to cases of marked, often anthropogenic, environmental change. Here we present the case of a small population of reed warblers (Acrocephalus scirpaceus) over a period of 19 years (1996-2014) after colonizing a restored wetland habitat in Malta. Our data show a population decrease in body mass, following a trajectory consistent with a population ascending an adaptive peak, a so-called Ornstein-Uhlenbeck process. We corroborate these findings with genetic and ecological data, revealing that individual survival is correlated with body mass, and more than half of the variation in mean population fitness is explained by variation in body mass. Despite a small effective population size, an adaptive response has taken place within a decade. A founder event from a large, genetically variable source population to the southern range margin of the reed warbler distribution likely facilitated this process.

Tempo does not correlate with mode in the fossil record.

The dominating view of evolution based on the fossil record is that established species remain more or less unaltered during their existence. Substantial evolution is on the other hand routinely reported for contemporary populations, and most quantitative traits show high potential for evolution. These contrasting observations on long- and short-time scales are often referred to as the paradox of stasis, which rests on the fundamental assumption that periods of morphological stasis in the fossil record represent minimal evolutionary change. Investigating 450 fossil time series, I demonstrate that the nonaccumulating morphological fluctuations during stasis travel similar distances in morphospace compared to lineages showing directional change. Hence, lineages showing stasis are commonly undergoing considerable amounts of evolution, but this evolution does not accumulate to produce large net evolutionary changes over time. Rates of evolutionary change across modes in the fossil record may be more homogenous than previously assumed and advocated, supporting the claim that substantial evolution is not exclusively or causally linked to the process of speciation. Instead of exemplifying minimal evolution, stasis likely represents information on the dynamics of the adaptive landscape on macroevolutionary time scales, including the persistence of adaptive zones and ecological niches over millions of years.

Interspecific interactions through 2 million years: are competitive outcomes predictable?

Ecological interactions affect the survival and reproduction of individuals. However, ecological interactions are notoriously difficult to measure in extinct populations, hindering our understanding of how the outcomes of interactions such as competition vary in time and influence long-term evolutionary changes. Here, the outcomes of spatial competition in a temporally continuous community over evolutionary timescales are presented for the first time. Our research domain is encrusting cheilostome bryozoans from the Wanganui Basin of New Zealand over a ca 2 Myr time period (Pleistocene to Recent). We find that a subset of species can be identified as consistent winners, and others as consistent losers, in the sense that they win or lose interspecific competitive encounters statistically more often than the null hypothesis of 50%. Most species do not improve or worsen in their competitive abilities through the 2 Myr period, but a minority of species are winners in some intervals and losers in others. We found that conspecifics tend to cluster spatially and interact more often than expected under a null hypothesis: most of these are stand-off interactions where the two colonies involved stopped growing at edges of encounter. Counterintuitively, competitive ability has no bearing on ecological dominance.

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.

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.