Respiratory medium and circulatory anatomy constrain size evolution in marine macrofauna

Abstract

The typical marine animal has increased in biovolume by more than two orders of magnitude since the beginning of the Cambrian, but the causes of this trend remain unknown. We test the hypothesis that the efficiency of intra-organism oxygen delivery is a major constraint on body-size evolution in marine animals. To test this hypothesis, we compiled a dataset comprising 13,723 marine animal genera spanning the Phanerozoic. We coded each genus according to its respiratory medium, circulatory anatomy, and feeding mode. In extant genera, we find that respiratory medium and circulatory anatomy explain more of the difference in size than feeding modes. Likewise, we find that most of the Phanerozoic increase in mean biovolume is accounted for by size increase in taxa that accomplish oxygen delivery through closed circulatory systems. During the Cambrian, water-breathing animals with closed circulatory systems were smaller, on average, than contemporaries with open circulatory systems. However, genera with closed circulatory systems superseded in size genera with open circulatory systems by the Middle Ordovician, as part of their Phanerozoic-long trend of increasing size. In a regression analysis, respiratory and circulatory anatomy explain far more size variation in the living fauna than do feeding modes, even after accounting for taxonomic affinity at the class level. These findings suggest that ecological and environmental drivers of the Phanerozoic increase in the mean size of marine animals operated within strong, anatomically determined constraints.

The evolution of complex life and the stabilization of the Earth system

“…Some taxa evolved open circulatory systems, while others evolved closed circulatory systems. Both systems appear to function well at the typical sizes of Cambrian animals [101], but circulatory systems appear to have constrained the later body size evolution of different higher taxa. The greater velocity and efficiency associated with closed circulatory systems permitted closed circulatory system taxa (especially chordates and cephalopods) to evolve to much larger body sizes later in the Phanerozoic, much more often than their relatives with open circulatory systems [101].…”

The gill-oxygen limitation theory (GOLT) and its critics

“…Note also that Eq. 6 also applies to WBE that lack gills and blood, as part of a closed system for distributing oxygen to the tissues (51). One such example is provided by the arrow worms (Chaetognatha), in which, in the absence of gills, the body integument serves as respiratory organ (52) and whose thickness cannot be reduced as they grow.…”

Respiratory protein-driven selectivity during the Permian-Triassic mass extinction

“… 26 Higher levels of O 2 -carrying proteins generally correspond to advanced circulatory and respiratory systems. 23 , 27 , 28 However, when investigating the significance of circulatory systems, we found that repository protein remained a more critical predictor of selectivity in extinction and size reduction ( Figure 2 ).…”