Evolvability and the Fossil Record

Abstract

The concept of evolvability—the capacity of a population to produce and maintain evolutionarily relevant variation—has become increasingly prominent in evolutionary biology. Although paleontology has a long history of investigating questions of evolvability, often invoking different but allied terminology, the study of evolvability in the fossil record has seemed intrinsically problematic. How can we surmount difficulties in disentangling whether the causes of evolutionary patterns arise from variational properties of traits or lineages rather than due to selection and ecological success? Despite these challenges, the fossil record is unique in offering growing sources of data that span millions of years and therefore capture evolutionary patterns of sustained duration and significance otherwise inaccessible to evolutionary biologists. Additionally, there are a variety of strategic possibilities for combining prominent neontological approaches to evolvability with those from paleontology. We illustrate three of these possibilities with quantitative genetics, evolutionary developmental biology, and phylogenetic models of macroevolution. In conclusion, we provide a methodological schema that focuses on the conceptualization, measurement, and testing of hypotheses to motivate and provide guidance for future empirical and theoretical studies of evolvability in the fossil record.

The developmental impacts of natural selection on human pelvic morphology

“…S1 and table S1) ( 3 ). Results from a large number of studies ( 28 – 33 ) [and see review by Love et al ( 33 )] have suggested that natural selection can affect patterns and magnitudes of variation and covariation among traits, and following previous work ( 32 , 34 ), we hypothesized that natural selection for parturition and bipedalism could affect patterns of morphological variation in the pelvis when humans are compared to African apes. While humans showed similar levels of variation in ischium length and acetabular diameter to other African apes, they showed less variation in iliac height and breadth, as well as pubis length, while gorillas and chimpanzees did not differ in those traits (Fig.…”

“…On the basis of the common assumption that the phenotypic variance/covariance matrix is proportional to the genetic variance/covariance matrix (see the Supplementary Materials and Methods) ( 33 , 35 ), as was done in numerous previous studies ( 32 , 34 , 36 – 40 ), we made this substitution and quantified the ability of a population to evolve in the direction of selection given stabilizing selection on other traits [i.e., conditional evolvability ( 34 ); see also the Supplementary Materials]. Our results show that humans have significantly lower levels of conditional evolvability than African apes in iliac breadth, pubis length, and acetabulum height, while ischium length displayed the opposite pattern (Fig.…”

“…Here, we substitute the phenotypic variance/covariance matrix (e.g., P ) for the genetic variance/covariance matrix (e.g., G ) based on the assumption that the two are proportional, a conjecture originally made by Cheverud (1988) ( 99 ) and later supported in a wide range of studies, particularly for morphological traits ( 35 ), and which has been done in numerous previous studies ( 32 , 33 , 37 , 39 , 40 , 100 ).…”

Aggregate trait evolvability and macroevolution in two sister species of the bryozoanStylopoma

“…However, heritability has fallen out of favor because is a measure that scales with the degree of phenotypic variance, and is therefore not an adequate quantitative prediction of evolutionary change across multiple traits (Houle, 1992). Instead, we scale additive genetic variance ( V A ) by the mean trait value squared, yielding a measure called evolvability (Houle, 1992; Hansen and Houle, 2008; Love et al, 2021). To estimate evolvability, first we calculated the covariances of these median and MAD values across parent and offspring colony generations to form a parent-offspring covariance matrix (Fernandez and Miller, 1985; Rice, 2004; Falconer and Mackay, 1996).…”

“…However, heritability has fallen out of favor because V A V P is a measure that scales with the degree of phenotypic variance, and is therefore not an adequate quantitative prediction of evolutionary change across multiple traits (Houle, 1992). Instead, we scale additive genetic variance (V A ) by the mean trait value squared, yielding a measure called evolvability (Houle, 1992;Hansen and Houle, 2008;Love et al, 2021).…”