The relationship between sternum variation and mode of locomotion in birds

Background The origin of powered avian flight was a locomotor innovation that expanded the ecological potential of maniraptoran dinosaurs, leading to remarkable variation in modern birds (Neornithes). The avian sternum is the anchor for the major flight muscles and, despite varying widely in morphology, has not been extensively studied from evolutionary or functional perspectives. We quantify sternal variation across a broad phylogenetic scope of birds using 3D geometric morphometrics methods. Using this comprehensive dataset, we apply phylogenetically informed regression approaches to test hypotheses of sternum size allometry and the correlation of sternal shape with both size and locomotory capabilities, including flightlessness and the highly varying flight and swimming styles of Neornithes. Results We find evidence for isometry of sternal size relative to body mass and document significant allometry of sternal shape alongside important correlations with locomotory capability, reflecting the effects of both body shape and musculoskeletal variation. Among these, we show that a large sternum with a deep or cranially projected sternal keel is necessary for powered flight in modern birds, that deeper sternal keels are correlated with slower but stronger flight, robust caudal sternal borders are associated with faster flapping styles, and that narrower sterna are associated with running abilities. Correlations between shape and locomotion are significant but show weak explanatory power, indicating that although sternal shape is broadly associated with locomotory ecology, other unexplored factors are also important. Conclusions These results display the ecological importance of the avian sternum for flight and locomotion by providing a novel understanding of sternum form and function in Neornithes. Our study lays the groundwork for estimating the locomotory abilities of paravian dinosaurs, the ancestors to Neornithes, by highlighting the importance of this critical element for avian flight, and will be useful for future work on the origin of flight along the dinosaur-bird lineage. Supplementary Information The online version contains supplementary material available at 10.1186/s12915-021-01105-1.

: Regression plots for testing for allometry along the first 4 PC axes. Test statistics provided in Table S1.  Figure S2: Sternal shape deformations showing the independent effect of sternum size and body size on sternum shape, showing smaller sizes in beige on the left and larger sizes in brown on the right. The grey shape overlain on the brown shape on the right (larger sternum size or body mass) represents the shape shown on the left side (smaller sternum size or body mass).

Figure S3
: Shape deformations showing the independent effects of forelimb propulsion and aerial flight. The light grey shape overlain on top of the coloured shapes represents the coloured shape that occurred to the left in the series as a baseline for comparison. Forelimb propulsion is associated with a longer sternal body and lower, anteriorly projected keel; aerial flight is associated with a shorter sternal body and taller, rounded keel.

LM1
Centre -The most anterior point of rostrum sterni. Sometimes this is confluent with the keel, sometimes it is separate.

SL1
Left -Side edge of rostrum sterni, landmarked from LM1 to LM2. Equivalent to SL2 on the right side.

LM2
Left -Corner between rostrum sterni and coracoid sulcus. Equivalent to LM3 on the right side.

SL2
Right -Side edge of rostrum sterni, landmarked from LM1 to LM3. Equivalent to SL1 on the left side.

LM3
Right -Corner between rostrum sterni and coracoid sulcus. Equivalent to LM2 on the left side.

LM4
Left -Most medial point of the left coracoid sulcus. Equivalent to LM6 on the right side.

LM5
Left -Most distal point of the left coracoid sulcus. Equivalent to LM7 on the right side.

LM6
Right -Most medial point of the right coracoid sulcus. Equivalent to LM4 on the left side.

LM7
Right -Most distal point of the right coracoid sulcus. Equivalent to LM5 on the left side.

LM8
Left -Corner/inflection point between main sternum body and left craniolateral notch.
Equivalent to LM9 on the right side.

SL3
Left -Perimeter of left craniolateral process, landmarked from LM8 until LM10. Equivalent to SL4 on the right side.

LM9
Right -Corner/inflection point between main sternum body and right craniolateral notch.
Equivalent to LM8 on the left side.

SL4
Right -Perimeter of right craniolateral process, landmarked from LM9 until LM12. Equivalent to SL3 on the left side.

LM10
Left -Anterior of anterior-most rib facet on the left side. Equivalent to LM12 on the right side.

LM11
Left -Posterior of posterior-most rib facet on the left side. Equivalent to LM13 on the right side.

LM12
Right -Anterior of anterior-most rib facet on the right side. Equivalent to LM10 on the left side.

LM13
Right -Posterior of posterior-most rib facet on the right side. Equivalent to LM11 on the left side.

SL5
Left -Lateral edge of sternum, landmarked from L11 to LM15. Equivalent to SL6 on right side.

SL6
Right -Lateral edge of sternum, landmarked from L13 to LM22. Equivalent to SL5 on left side.

LM14
Centre -Midpoint of sternum on posterior edge in ventral view.

LM15
Left -Caudolateral distal corner of sternum, or of lateral trabecula when present. Equivalent to L22 on right side.  Equivalent to LM28 on the right side.

LM22
Right -Caudolateral distal corner of sternum, or of lateral trabecula, when present. Equivalent to L15 on left side.

LM23
Right -Medial corner of lateral trabecula when present. If a lateral trabecula is absent, place a series of semi-landmarks between the last landmark that was placed (eg. LM22) and LM14 and skip the remaining landmarks of the posterior border on the right side (LM24-28), as they are later estimated as equidistant midpoints derived from this semi-landmark series. If a fenestra is present, it should be treated as a lateral trabecula that has fused; this landmark should be placed along the posterior border directly posterior to the midpoint of the fenestra. Equivalent to LM16 on the left side.

LM24
Right -Most anterior point of the most distal sternal notch (if two notches are present; if only one notch is present, this landmark denotes it). If this notch is absent, place a series of semilandmarks between the last landmark that was placed and LM14, and skip the remaining landmarks of the posterior border on the right side (LM25-28), as they are later estimated as equidistant midpoints derived from this semi-landmark series. If a fenestra is present, it should be treated as a lateral trabecula that has fused; this landmark should be placed on the most anterior point of the fenestra. Equivalent to LM17 on the left side.  Equivalent to LM21 on the left side.

LM29
Left -Most posterior corner of sternal keel. Equivalent to LM30 on the right side.

SL7
Left -Perimeter of sternal keel, landmarked from LM29 to LM1. Equivalent to SL8 on right side.

LM30
Right -Most posterior corner of sternal keel. Equivalent to LM29 on the left side.

SL8
Right -Perimeter of sternal keel, landmarked from LM30 to LM1. Equivalent to SL7 on left side.

LM31
Centre -Midpoint of sternum on posterior edge in dorsal view.