The Emergence of Whales, Chp. 13

Synopsis of Chapter 13: Evolution of Thermoregulatory Function in Cetacean Reproductive Systems

D. Ann Pabst, Sentiel A. Rommel, and William A. McLellan

DP and WM: Biological Sciences and Center for Marine Science Research, University of North Carolina-Wilmington, Wilmington, NC 28403

SR: Marine Mammal Pathobiology Laboratory, Florida Marine Research Institute, FL Dept. of Environmental Protection, St. Petersburg, FL 33711 (located next to my grad school!)

1. INTRODUCTION

1st sentence: “Modern cetaceans possess a suite of morphological adaptations (!!) that permit their existence in the marine environment.” Body streamlining, musculoskeletal system, blubber, and dorsal fin and flukes allow efficient swimming and whole body thermoregulation.

Some adaptations might appear to threaten the temperature-sensitive reproductive tissues. Males have intra-abdominal testes, an aid to streamlining. BUT, the testes are located tightly between the “thermogenic” axial and abdominal locomotor muscles. Could cause exposure to core or above-core temperatures.

Many mammals require sperm production at below-core temps. Temps between 35-38 C can block spermatogenesis or affect long-term storage. Usual solution is physical separation from the body core via scrota. Plus, cetaceans have high core temps.

For females, same problems, potentially producing high uterine temps that could affect fetal development. Fetal metabolic rate can be 2x maternal, so heat must be transferred from fetus to mother, and any block to heat transfer can excessive fetal temps — which is bad (resulting conditions cited).

Discussion of where the fetal heat goes: 85% to the placenta, then to maternal environment and external environment. 15% to uterine fluids, then to external environment via abdominal wall.

THIS IS JUST SO COOL (HA): So how do cetaceans thermoregulate the reproductive system? They have a novel vascular system featuring a countercurrent heat exchanger (CCHE). The CCHE brings cooled venous blood from the fins to an area where the arteries that supply the reproductive tissues are located.

Chapter will describe the CCHE, showing that it works as advertised, and then show the relationship of cetacean reproductive system to other members of clade Artiodactyla. I.e., “the majority of reproductive structures reflect cetacean phylogenetic relationships and not novel adaptations to a marine environment.” The unique features of the reproductive system are paedomorphic (retained juvenile structures). Thus, the “apparently complex suite of morphological changes that occurred during the evolution of cetaceans from a terrestrial to an aquatic form may be parsimoniously explained as representing a suite of arrested embryonic characters in the adult.”

2. REPRODUCTIVE MORPHOLOGY OF CETACEANS

2.1 Males PARENTAL WARNING: Mature content

Diagram provided. Testes are in the caudal abdominal cavity. Each is attached to the abdominal wall via a mesorchium that connects to the testis along the epididymal border. Epididymis runs along the testis to the ductus deferens. One accessory gland, the prostate. The urethra travels through a “poorly developed” corpus spongiosum. The penis can be retracted into the body wall, and is fibroelastic like most artiodactyls. The nonerect penis is curved into a sigmoid flexure in the body wall (as in ruminants). The penis straightens and becomes turgid on erection, but does not change length or diameter. The retractor penis muscle location is similar to ruminants. Two functions are possible: maintenance of the position of the nonerect penis in the prepuce, and also as a “brake in regulating the stretching of the penis during erection.”

2.2 Females

Ovaries are surrounded by “fimbriae” (SCRABBLE alert) of a distal uterine tube, which joins a horn of the cetacean bicornuate uterus. Everything held in place by an extensive mesentery called the broad ligament (3 regions with various necessary attachments).

Placenta is like artiodactyls; uterus terminates at a muscular, true cervix. Distal to the true cervix, the wall of the vaginal canal has annular folds called pseudocervices, unique to cetaceans: called “a remarkable anatomical adaptation for breeding in the marine environment”. Some writers thought they were unique to cetaceans but they are also found in (think hard) cows and sows. Final details: the vaginal canal terminates at the vulva, within a slit-shaped aperture in the body wall. The external genitalia include labia minora, labia majora, and a “well-developed clitoris”.

(That’s just about all I need to know on that subject.)

3. VASCULAR STRUCTURES ASSOCIATED WITH CETACEAN REPRODUCTIVE SYSTEM

The vascular structures for cetacean reproductive tissues are homologous with other tetrapod mammals. The lumbocaudal venous plexus (to be described) which “is independent of, but juxtaposed to, the arterial supply to the reproductive tissues, is unique to cetaceans.” The arterior and venous vessels form the CCHE, which can cool the testes and uterus.

Male and female systems will be described separately. Descriptions are based on >30 dissections of stranded or fishing-related deaths of dolphins, pilot whales, and fin whales. Some structures have been previously described, but the countercurrent vascular system “has not been previously identified”.

SO THIS IS GROUNDBREAKING STUFF, LADIES AND GENTS.

3.1 Males

3.1.1 Spermatic and Testicular Arteries and Veins

Blood supply to the testis via the spermatic arterial plexus (SAP), from the dorsal aorta. Unlike other mammals, 40 individual spermatic arteries leave the aorta. They are convoluted leaving the aorta, but straighten toward the testis, and become organized into a single layer with parallel orientation. This is the SAP.

Near the SAP ventrolateral margin, the arteries coalesce into a cone- shaped mass, which anastomoses into fewer, larger-diameter arteries as the cone tapers caudally. At the terminus, a single testicular artery enters the tunic of the testis. A few branches feed the epididymis. (The SAP is less developed in sexually immature males.)

Figure 4 illustrates all of this. It’s a great and easy to understand figure. Holy heat exchanger, Batman!

The testis is drained by testicular veins, which go to the venae cavae.

3.1.2. Lumbocaudal Venous Plexus (LVP)

(Gets really interesting here.) Spermatic and testicular arteries and veins are homologous to other tetrapods. The LVP is the other novel testicular structure. It’s composed of anastomosed, thin-walled vessels in a connective tissue membrane. It lies dorsolateral and juxtaposed with the SAP, putting veins and arteries in close proximity.

The LVP gets venous blood draining the dorsal fin and fluke. Networks of veins in both fin and fluke coalesce into larger-diameter veins inside the blubber layer to the LVP. Venous blood is cooled by exposure to ambient water in the fin and flukes, and this cooled blood is distributed along the dorsolateral wall next to the SAP by the LVP.

Does it work? First, the female structure.

3.2 Females

3.2.1 Uterovarian Venous Plexus

Most other mammals have two or three vessels; the uterovarian veins and arteries in cetaceans are flattened plexuses. 2 separate regions: proximal to the dorsal midline, and with the mesometrium. The proximal region is less anastomosed than the mesometrial region. The mesometrium wraps around the lateral margin of the uterus and attaches to the ventrolateral margin of the uterine horn, similar to the testes arrangement in males.

Approximately 20-40 arterial branches form exiting the aorta. The arterial plexus lies juxtaposed to the venous plexus. Similarly, the venous plexus has 20-40 veins. The discrete vessels here contrast with the irregular anastomosing channels in the LVP. The CCHE is similar to the males, a proximal region of the uterovarian arterial and venous plexuses.

4. FUNCTION OF THE CCHE IN TURSIOPS TRUNCATUS

Because the CCHE flanks the bowel and influences colonic temperatures, the function of it can be checked indirectly. A linear array of thermocouples placed in the bowel was used to investigate the temperature distribution. Demonstrated temps were 0.2-0.7 C cooler next to the CCHE in a prepubescent male, and 0.9-1.3 C cooler in a sexually mature male. Temperatures decrease with exercise in the CCHE region, likely due to increased venous blood flow.

5. EVOLUTIONARY HYPOTHESIS: THE CCHE IS A PAEDOMORPHIC VASCULAR DESIGN

Starting with the premise that cetaceans are sister taxa to ungulates (the authors leave open the possibility of Chapter 4, that cetaceans are highly-derived ungulates/artiodactyls), they do a small phylogenetic tree between artiodactyls and cetaceans based on the reproductive system. Artiodactyla and Cetacea have pseudocervices and a fibroelastic penis (you can figure out which gender has which, I hope); cetaceans uniguely possess intra-abdominal testes, pelvic vestiges***, the spermatic or uterovarian arterial plexuses, and the lumbocaudal venous plexus.

*** Don’t miss the discussion of this coming up!

So the hypothesis is that the unique characters are paedomorphic, i.e. arrested embryonic characters “retained and specialized in the adult”.

1. Testis position. During embryonic or early postnatal development, the testes descend from the abdominal cavity to the scrotum (it’s not good for baby boys if this doesn’t happen). The gubernaculum (SCRABBLE alert) is critical to the descent of the testes, and some odontocetes have it in fetal development; fin whales may have a vestigial inguinal canal; but the intra-abdominal position of the testes can be considered an arrested embryonic character.

2. Pelvic vestiges. In tetrapods, the 3 pelvic bones develop from a cartilaginous template. The exact identity of the elements of the pelvic vestige in cetaceans has not been established. The crura of the penis are anchored to the pelvic vestiges, so they hypothesize that the vestiges are an arrested developmental state of the ischium.

*** READ THIS. Quote provided in entirety.:

“Note: The pelvic bones of cetaceans are usually described as vestiges (Rommel, 1990) to denote that they are the product of a reduction from the condition found in their ancestors. The hypothesis presented here – that these bones represent an arrested embryonic condition – supports the usage of the term pelvic _rudiment_ (sensu van der Schoot, 1990) rather than vestige.”

3. SAP and uterovarian plexuses. Early in development, blood to gonads via multiple vessels; the majority disappear later in development. As described above, arterial blood supply to the testis/ovary and uterus is via the plexuses, i.e., multiple vessels. Suggest that this is a hypertrophied embryonic condition in the adult.

4. LVP intervening between cutaneous veins and duplicated venae cavae. Early vascular development shows networks/plexuses of capillaries. Larger vessels emerge during development. Early development also has extensive connections between deep and superficial vessels. As before, the existing plexuses are proposed to be retained embryonic characters. [Supporting references]

Good question: fins and flukes are new: how did evolution set up the connections that get the cooled venous blood from the fins and flukes? The connections between deep and superficial vessels are embryonic, but it’s critical to “wire” into the fins and flukes.

Suggest further investigation of reproductive organ development to test the paedomorphic hypothesis. They also suggest comparative studies of the reproductive and vascular anatomy of finless cetaceans. (Challenge to the readers: name a finless cetacean. I can’t.)

6. Summary

Exactly that. Nothing new or surprising.

With 3 chapters remaining (the last two being the really fun ones), we can still look forward to Chapter 14,

“Isotopic Approaches to Understanding the Terrestrial-to-Marine Transition of the Earliest Cetaceans”

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