Size as a Line of Least Evolutionary Resistance: Diet and Adaptive Morphological Radiation in New World Monkeys

Abstract

New World monkeys (NWM) display substantial variation (two orders of magnitude) in body size. Despite this, variation in skull size and associated shape show a conserved allometric relationship, both within and between genera. Maximum likelihood estimates of quantitative ancestral states were used to compare the direction of morphological differentiation with the phenotypic (p(max)) and genetic (g(max)) lines of least evolutionary resistance (LLER). Diversification in NWM skulls occurred principally along the LLER defined by size variation. We also obtained measures of morphological amount and pace of change using our skull data together with published genetic distances to test whether the LLER influenced the amount and pace of diversification. Moreover, data on an ecological factor (diet) was obtained from the literature and used to test the association of this niche-related measure with the morphological diversification. Two strategies were used to test the association of LLER with the morphological and dietary amount and pace of change, one focusing on both contemporary genera and maximum likelihood reconstructed ancestors and the other using only the 16 contemporary genera in a phylogenetic comparative analysis. Our results suggest that the LLER influenced the path, amount, and pace of morphological change. Evolution also occurred away from the LLER in some taxa but this occurred at a slower pace and resulted in a relatively low amount of morphological change. We found that longer branch lengths (time) are associated with larger differences in p(max) orientation. However, on a macroevolutionary scale there is no such trend. Diet is consistently associated with both absolute size differences and morphological integration patterns, and we suggest that this ecological factor might be driving adaptive radiation in NWM. Invasion of diet-based adaptive zones involves changes in absolute size, due to metabolic and foraging constraints, resulting in simple allometric skull diversification along the LLER. While it is clear that evolutionary change occurred along the LLER, it is not clear whether this macroevolutionary pattern results from a conservation of within-population genetic covariance patterns or long-term adaptation along a size dimension or whether both constraints and selection were inextricably involved.

The evolution of phenotypic integration: How directional selection reshapes covariation in mice

“…2009). Our results suggest that these difference can be explained by the pervasiveness of selection on size along the mammalian clade (Marroig and Cheverud 2005; Baker et al. 2015).…”

Morphological divergence in a continental adaptive radiation: South American ovenbirds of the genusCinclodes

“…Body Size, Morphological Evolution, and Taxonomic Consequences Divergence in body size among adaptively radiating taxa is relatively well documented and appears to be the primary axis of divergence in multiple systems (Nagel and Schluter 1998, Marroig and Cheverud 2005, Claramunt 2010). Cinclodes shows similarly strong divergence in body size.…”

“…We hypothesized that species of this genus may also be morphologically diverse, given their documented ecological and physiological diversity. Many taxa have diverged primarily in body size (Ricklefs and Travis 1980, Beuttell and Losos 1999, Marroig and Cheverud 2005, Claramunt 2010, and therefore we predicted that body size would account for the majority of morphological diversity among Cinclodes species. However, because Cinclodes species also have diverse migratory habits Martínez del Rio 2005, Martínez del Rio et al 2009) and vary in elevational range and diet (Chesser 2004, Sabat et al 2006b, Martínez del Rio et al 2009), we also expected variability in wing (Lockwood et al 1998) and bill size and shape.…”

Biogeographic variations in wood mice: testing for the role of morphological variation as a line of least resistance to evolution

“…Size --related shape changes have been suggested, and indeed demonstrated as a line of least resistance to evolution in bony traits such as skull and mandible (Marroig and Cheverud 2005;Cardini and Thorington 2006). Such traits are prone to change along growth due to bone remodeling, making of intra--population allometry a significant component to Pmax (Renaud and Auffray 2013).…”

“…Pmax can thus be studied in wild populations (e.g. Ackermann and Cheverud 2000;Marroig and Cheverud 2005) and even in fossils (e.g. Renaud et al 2006;Hunt 2007).…”